Three-way fungal interactions affect the potential biological control of Himalayan balsam,Impatiens glandulifera

Himalayan balsam (Impatiens glandulifera) is one of the most invasive weeds across Europe. The rust fungus, Puccinia komarovii var. glanduliferae has been introduced as a biological control agent, but success has been patchy. Here, we investigated whether mycorrhizal and endophytic fungi can affect rust efficacy and plant growth. Over three experiments, we found that AM fungi and the rust alone or together consistently reduced plant growth, but this depended on the identity of species in the AM inoculum. Meanwhile, AM fungi increased infection frequency of the endophyte Colletotrichum acutatum. Rust inoculation had no detrimental effects on mycorrhizal colonisation or C. acutatum infection, but the latter two fungi reduced rust sporulation. However, plant size was reduced when all three fungal types were present, suggesting that a combined fungal inoculum offers a promising approach for the control of this weed.     

First release of a fungal classical biocontrol agent against an invasive alien weed in Europe: biology of the rust,Puccinia komarovii var. glanduliferae

The rust fungus Puccinia komarovii var. glanduliferae was first identified infecting Impatiens glandulifera in its native range (western Himalayas) between 2006 and 2010. Subsequently, it was imported into quarantine in the UK for evaluation as a classical biocontrol agent. To assess the safety of the rust, plant species relevant to Europe were tested for susceptibility. To confirm the life cycle, all infective spore stages were inoculated on I. glandulifera to follow disease progression. Teliospores were primed using bleaching and low temperatures to break dormancy. Temperature and dew period experiments using urediniospores were conducted to assess the parameters required for infection. Of the 74 plant species tested, only I. balsamina, an ornamental species, was fully susceptible to urediniospore inoculum. The life cycle of the rust – an autoecious, full‐cycled species with five spore stages – was confirmed. Urediniospores were infective between 5 and 25°C, with an optimum at 15°C. A minimum of 8 h dew period was required to achieve consistent infection. Based on a pest risk assessment, the rust poses no threat to native biodiversity within EU Member States; making P. komarovii var. glanduliferae a suitable candidate as the first fungal classical biocontrol agent against an exotic weed in the region.     

Positive plant–soil feedbacks of the invasive Impatiens glandulifera and their effects on above‐ground microbial communities

Impatiens glandulifera is one of the most widespread invasive plant species in the UK. Although aspects of its biology are known, there is little information about its association with microbial communities, both above ground and below ground. Furthermore, it is unknown whether this species exhibits any form of plant–soil feedback (PSF), commonly seen in other invasive weeds. We conducted a PSF experiment, in which plants of I. glandulifera were grown in soil that supported the species and compared with plants grown in a control soil from the same locality. Soil nutrients were measured, and the soil and foliar microbial communities were assessed. Impatiens glandulifera grew larger and faster in conditioned soil compared with the control. Higher levels of phosphate were also found in conditioned soils. Arbuscular mycorrhizal fungal (AMF) colonisation was lower in conditioned soils, suggesting that I. glandulifera may rapidly alter AMF communities in invaded areas. PSFs had a significant effect on the foliar endophyte community, with clear separation of species between conditioned and control soils. These results show that I. glandulifera displayed a positive PSF and the PSF mechanism extended beyond the soil microbial community to affect foliar endophytes. The observed increase in endophytes in plants grown in conditioned soil could enhance resistance to herbivory, thus further accentuating the invasive properties of this species.     

Endophytic fungi in the invasive weed Impatiens glandulifera: a barrier to classical biological control?

The rust fungus, Puccinia komarovii var. glanduliferae, has been introduced into the UK for biological control of the invasive weed, Impatiens glandulifera (Himalayan balsam). However, establishment of the pathogen has differed across the country, which may be partly explained by variation in plant genotype. The aim of this study was to examine whether there is a further layer of phenotypic resistance, provided by indigenous foliar endophytic fungi. Culturable endophytes were isolated from a number of different balsam populations, and the commonest species were inoculated into ‘clean’ balsam plants, to test their interactions with the rust. We found that endophyte communities within balsam are low in diversity and become more dissimilar with increasing distance between populations. Three endophytes (Colletotrichum acutatum, Alternaria alternata and Cladosporium oxysporum) were common and appeared to be antagonistic to the rust, reducing pustule number and mitigating the effect of the pathogen on plant biomass. I. glandulifera thus partially conforms to the endophyte-enemy release hypothesis, in that as an introduced species, it has an impoverished endophyte complement, acquired from the local environment. However, these endophytes represent a potential barrier to effective biological control and future weed control strategies need to find strains of rust that can overcome plant genetic resistance and the overlaying phenotypic resistance, conferred by endophytes. Future classical biological control programmes of weeds must therefore take into account the fungal bodyguards that invasive species may acquire in their introduced ranges.     

The regulation of biological control of weeds in Europe – an evolving landscape

After a difficult start, classical biological control of weeds is becoming recognized as an option for management of invasive plants in European Union (EU) Member States with intentional releases in three countries over the past 5 years. Many European countries are benefitting from the presence of Stenopelmus rufinasus, the azolla weevil, which has been accidentally introduced to the region. However, the UK experience with the official release of the psyllid Aphalara itadori against Japanese knotweed (Fallopia japonica) and the subsequent release of the rust Puccinia komarovii var glanduliferae against Impatiens glandulifera showed the regulatory framework that could be followed by EU Member States. This process was followed in advance of the subsequent release of Trichilogaster acaciaelongifoliae, a specific Australian bud‐galling wasp, against the invasive Acacia longifolia in Portugal. Soon the case of Ophraella communa, another accidental introduction that is severely limiting Ambrosia artemisiifolia populations, will influence affected countries, some of which have been uninterested in this technique until now, to consider the advantages and disadvantages of classical biocontrol. The future looks bright for classical weed biocontrol and the EU Regulation on Invasive Species should further aid this situation.     

Patterns of loss of biodiversity associated with invasion by Chrysanthemoides monilifera subsp. monilifera (boneseed) across a large geographic region

To investigate the impact of invasion by Chrysanthemoides monilifera ssp. monilifera (boneseed) on plant communities, sites that were invaded and uninvaded were surveyed across Tasmania, South Australia and Victoria, Australia. Above‐ground cover abundance was estimated and samples of the seed bank from invaded and uninvaded sites in each state were collected and germinated in the glasshouse. We compared species richness and composition between invaded and uninvaded sites for both above‐ground and below‐ground samples. Across this broad geographic area, C. monilifera invaded sites had 25% fewer species than uninvaded sites and twice as many exotic species. Most growth forms showed reduced richness in invaded sites. There were no differences in the composition of native species communities between invaded and uninvaded sites in most regions, except South Australia. The composition of the seed bank differed from the above‐ground vegetation, but was similar within each state. Herbs and grasses were most abundant. The species composition of the seed bank was different in invaded sites only in Victoria, suggesting that invasion may negatively influence the capacity of the seed bank to restore vegetation in some areas. However, the underlying mechanisms for the observed patterns were not tested in this study. The capacity of all sites to regenerate effectively from the seed bank was limited and, in order to ensure the conservation of biodiversity into the future, monitoring of species richness at smaller scales, particularly those where management of C. monilifera has occurred, will be needed to ensure management can facilitate the establishment of missing species. This study suggests that C. monilifera impacts a range of functional groups and different species across its distribution and is therefore non‐selective in how it influences changes in communities.     

Potential of a coevolved rust fungus for the management of Himalayan balsam in the British Isles: first field releases

In 2014, the rust fungus Puccinia komarovii var. glanduliferae, native to the foothills of the Himalayas from Kashmir to Western Nepal, became the first fungal agent to be released into Europe for the classical biological control of a non-native weed. The target, Impatiens glandulifera or Himalayan balsam, is a prolific invader of riparian habitats in Europe and North America. During the period 2015–2018, a strain of the rust from India was released at a total of 36 sites, in 17 counties in England and Wales. There was limited field infection in 2015 and inoculation experiments conducted under controlled conditions revealed significant variation in the susceptibility of plant populations to the rust, with some showing immunity. Subsequently, a second strain of the rust from Pakistan was released in 2017 and was found to infect a different cohort of Himalayan balsam populations. The rust mass production methodology, and field inoculation and monitoring protocol, are detailed, and plants were tested for susceptibility to both rust strains prior to field release. Levels of foliar infection at selected sites in 2017 and 2018 are presented, as well as seedling infection rates in the spring of 2019. The results show that the rust is able to overwinter and establish populations in stands of Himalayan balsam in England. The issues involved with measuring the impact of the biological control agent are discussed.     

The invasive Impatiens glandulifera Royle (Himalayan balsam) in the Republic of Macedonia: first record and forecast

A population of Impatiens glandulifera Royle, an invasive plant species native to the Western Himalayas, was recorded in 2013 near the village Gorno Sedlarce in the north‐western mountainous region of the Republic of Macedonia. I. glandulifera is a new alien species to the Macedonian flora. The surveys revealed an intensive growth and a low to medium density population of I. glandulifera. The population's density was not quantified, but several stands of different sizes were found. A rapid ecological risk assessment, mainly based on knowledge about invasion histories in North–Western and Central European countries, showed that this species, which is on the EPPO List of Invasive Alien Plants, is a serious threat to Macedonian biodiversity. Biological invasions of I. glandulifera affect biodiversity worldwide, and, consequently, the invaded ecosystems may experience significant losses in economic and cultural values. There is a clear need to develop a strategy for control of I. glandulifera to protect biodiversity, as a whole.     

Spread of Impatiens glandulifera from riparian habitats to forests and its associated impacts: insights from a new invasion

Impatiens glandulifera is a globally successful invader that primarily spreads along riparian habitats; however, during the last ~20 years, it has started to colonise forests, but little has been published on impacts of this recent spread. Several factors may have contributed to this phenomenon: (i) high propagule pressure from large and widespread riparian populations, (ii) extensive anthropogenic and natural disturbances in the forest ecosystems, (iii) increased use of forest machinery efficiently spreading the seeds together with (iv) a wide environmental tolerance of the species. The impacts of I. glandulifera on native communities in forests are manifold. Contrasting effects are reported on native plant species diversity, richness and growth of saplings of co-occurring species, as well as negative effects on soil mycorrhizal fungi. We suggest that the eradication of I. glandulifera populations in forests is more feasible than along watercourses because the recolonisation in forests is limited and, in some cases, populations are outcompeted by woody species during succession.     

Growth traits of the exotic plant Hydrocotyle vulgaris and the evenness of resident plant communities are mediated by community age,not species diversity

Biological invasions are determined by interactions between resident plant communities and exotic plants. Time of invasion and species diversity of resident plant communities may greatly affect exotic plant invasions. We assembled low‐ and high‐diversity resident plant communities by sowing seeds of four and eight grassland species, respectively, and at each of three time periods (1, 4 and 7 weeks after sowing), the resident communities were invaded by Hydrocotyle vulgaris or not. We also constructed a plant community with H. vulgaris alone. Presence of H. vulgaris had no effect on biomass of the resident communities or biomass of each component species. Community age significantly affected biomass and evenness of the resident communities, and their competition with H. vulgaris, but the priority effect of the resident communities was slight. Increasing species richness did not change the interaction between H. vulgaris and the resident plant communities. These findings suggest a weaker competitive exclusionary effect of H. vulgaris on the resident communities with early germination, and H. vulgaris tended to have no significant impact on intact resident terrestrial plant communities. Thus, the potential risk of H. vulgaris invasion is low, especially in the communities with young age.     

Effect of cutting frequency on above‐ and belowground biomass production of Rumex alpinus,R. crispus,R. obtusifolius and the Rumex hybrid (R. patienta × R. tianschanicus) in the seeding year

Rumex species are important weeds in grasslands and on arable land. The Rumex hybrid (R. patienta × R. tianschanicus; cv. OK‐2, Uteusha) has been planted as a forage and energy crop since 2001 in the Czech Republic, but its ecological requirements and its potential to become a new weedy species have never been investigated. In 2010 and 2011, we performed a pot experiment to investigate the effect of none, one and two cuts per year on biomass production of Rumex OK‐2 and common broad‐leaved Rumex species (Rumex obtusifolius, R. crispus and R. alpinus). The higher cutting frequency can reduce the belowground biomass, but no effect on the aboveground biomass was detected. Flowering in the seeding year was recorded in only 50% of R. obtusifolius plants. Non‐flowering R. obtusifolius plants produced significantly more belowground biomass than flowering plants under no cutting or one cut treatments. The growth response of Rumex OK‐2 to different cutting treatments was very similar to R. crispus. These similarities indicate the weed potential of the hybrid to become a troublesome weedy species, similar to R. crispus.     

Mycorrhiza induced resistance in potato plantlets challenged by Phytophthora infestans

Biological control of soil-borne pathogens by arbuscular mycorrhizal (AM) fungi has been repeatedly demonstrated. However, their role in the control of above-ground hemibiotrophic pathogens is less conclusive. Here, we investigated in vitro the impact of an AM fungus on Phytophthora infestans in potato plants. The leaf infection index was decreased in mycorrhizal potato plants. Real-Time Quantitative PCR revealed the induction of two pathogenesis related genes (PR1 and PR2) in the leaves of mycorrhizal plants shortly after infection with P. infestans. These results suggested a systemic resistance in mycorrhizal plants, related to the priming of the two PR genes in potato.     

Shade-induced plasticity in invasive Impatiens glandulifera populations

Phenotypic plasticity, which confers a fitness advantage under heterogeneous and novel environments, has been commonly suggested to contribute to the success of invasive plants in their introduced range. For example, plasticity in response to changes in light availability could facilitate invasiveness by allowing plants to both rapidly establish in unshaded, disturbed habitats, and tolerate shaded or crowded environments. The plastic responses of invasive plants to shade were mostly studied in morphological traits. However, plasticity in physiological traits might provide more rapid and reversible responses and thus be more effective in environments with rapid temporal variations. Here, we compared plasticity in a range of morphological and physiological traits that provide shade avoidance or tolerance between two native and six introduced populations of Impatiens glandulifera. In a common garden, we subjected second-generation siblings of native and invasive plants to two light availability treatments and measured their morphological, physiological and performance responses. Impatiens glandulifera from invasive populations exhibited greater phenotypic plasticity in response to light availability in four out of 12 measured traits. Moreover, this greater plasticity was mostly limited to physiological traits associated with photosynthetic acclimation. These results suggest high phenotypic plasticity in response to light availability could have facilitated I. glandulifera's spread in both disturbed habitats and woodlands or under intense light competition. The results of this study highlight the importance of considering physiological traits when studying the role of plasticity in the success of invasive plants.     

Plant invasiveness and target plant density: high densities of native Schima wallichii seedlings reduce negative effects of invasive Ageratina adenophora

Economically feasible strategies to cope with invasive species are urgently needed. Plant density can be increased to reduce competitive effects on target plants. This study indicates that increasing native plant density can be used to reduce the effect of invasive Ageratina adenophora. Seedlings of an indigenous tree species, Schima wallichii, were grown in pots containing uninvaded or invaded soil, with or without A. adenophora leaf litter on the soil surface. Schima wallichii seedlings were also grown at four densities under four levels of A. adenophora leaf litter. Root and shoot biomass and length were measured as response parameters in both bioassays. Schima wallichii growth was inhibited by A. adenophora leaf litter and invaded soil. High litter levels reduced S. wallichii root length and dry weight at low plant densities. The inhibition disappeared at high S. wallichii plant densities. As A. adenophora did not inhibit S. wallichii growth at high plant densities, adjustments of seedling density should be studied as a possible management strategy for invasion by A. adenophora and potentially by other exotic plant species. As density‐dependent growth inhibition is the key characteristic of chemical interference, we propose that phytotoxins contribute to A. adenophora invasion particularly at low densities of native seedlings.     

Biology and management of the invasive weed Ageratina adenophora (Asteraceae): current state of knowledge and future research needs

Biological invasion is increasing worldwide and the management of invasive species is becoming an important priority for vegetation managers. Success of invasive species management depends on a thorough understanding of the biology of the organism in question and the effectiveness of current management efforts, in order to identify the best practices for management improvement. In this review, we synthesised current biological knowledge of a noxious invasive weed Ageratina adenophora to identify knowledge gaps and assessed management efforts to identify best practices. Finally, we proposed some priority areas for future research to fill knowledge gaps and improve management. Our analysis showed that A. adenophora has already invaded 40 countries, mainly in Asia, Oceania, Africa and Europe. Phenotypic plasticity, allelopathic interference and invasion‐mediated changes in the soil microbial community are the proposed mechanisms that facilitate rapid spread of this weed. However, allelopathy as a mechanism of invasion success of this weed has not been supported by ecologically meaningful experiments. Though mechanical, chemical and biological control measures have been used, their success remains limited and the weed continues to spread in new regions. Among seven biological control agents examined to date, gall fly (Procecidochares utilis) and leaf spot fungus (Passalora ageratinae) have been effective in limited areas to suppress growth of this weed. Some perennial native grasses (e.g. Setaria sphacellata and Lolium perenne) have shown potential to competitively suppress A. adenophora. In conclusion, understanding the invasion mechanisms, exploring further to identify effective biological control agents, combined with approaches of ecological restoration, could help in the management of this weed.     

The effects of the herbicide metsulfuron-methyl on litter invertebrate communities in a coastal dune invaded by Chrysanthemoides monilifera spp. rotundata

We investigated the impacts of application of the sulfonylurea herbicide, metsulfuron-methyl, on soil and litter invertebrates in coastal vegetation where the weed Chrysanthemoides monilifera has invaded. We followed changes in litter invertebrates for 125 days following treatment to investigate direct toxic and indirect effects of treatment. Overall we found no effect of treatment on abundance, taxonomic richness or composition of litter invertebrates. In general, abundance and richness declined with time in both treated and untreated sites, suggesting that climatic factors were far more important in determining invertebrate communities than the effects of the treatment. Even changes in cover of vegetation as a result of death of the weed resulted in few measurable effects on invertebrates. It is concluded that metsulfuron-methyl had no impact on invertebrate communities up to 125 days following treatment.     

Parthenium hysterophorus in Nepal: a review of its weed status and possibilities for management

The rapid expansion of the alien invasive Parthenium hysterophorus is a new agricultural and environmental problem for Nepal. Although the weed was first recorded in 1967, the most significant expansion has occurred in the last 20 years. The weed is thought to have entered Nepal from India and currently is found in the Tarai, Siwalik and hill regions of Nepal. A CLIMEX modelling projection has shown these regions to be climatically suitable for the growth of P. hysterophorus, both under the present and a future projected increased temperature. From the initially invaded roadside vegetation, the weed has now spread into cropping land and forests. Vehicle movement and transportation of agriculture products are the main means by which its seed is spreading. The weed has reduced plant species richness and changed species composition in grasslands, while fodder collectors have developed contact dermatitis from the plant. To date, no sustainable management strategy has been developed for this weed. However, the fortuitous arrival of the biological control agents Zygogramma bicolorata and Puccinia abrupta var. partheniicola has had some impact upon the weed's growth and abundance. A CLIMEX modelling projection identifies many suitable locations for Z. bicolorata outside of its present range and within areas where the weed is likely to spread, both under the present and under a future projected climate of increased temperature. Mapping of the currently invaded areas, management through community involvement and further releases of new and redistribution of current biological control agents are required to manage P. hysterophorus in Nepal.     

The role of community composition in grassland response to two methods of exotic forb removal

Invasive plants can seriously threaten biodiversity and ecosystem function. Thus, controlling the abundance and mitigating the deleterious effects of invasive plants is imperative. The effectiveness of removal methods could vary based on potential damage to non‐target species and on the ecological context of invasion. For example, species‐poor communities might benefit disproportionately from invasive removal because they tend to be more heavily invaded than species‐rich communities. In this study, we tested the efficacy of two common methods of invasive plant control, hand removal and 2,4‐D herbicide application, against the invasive forb, Galium verum. We further tested whether the community response to G. verum removal varied across communities that differed in native grass richness (one, three or six species) and composition. Grass diversity did not interact with G. verum removal to influence any response. Instead, hand removal and herbicide application each reduced G. verum stem density by >50% relative to controls. Furthermore, hand removal of G. verum increased species richness by 25% relative to controls and herbicide‐sprayed plots. Despite this benefit, hand removal is labour‐intensive and impractical for large areas. These results also suggest that applying herbicide may control G. verum spread without substantially reducing forb diversity in invaded tallgrass prairie. Thus, herbicide application may be most suitable for grasslands with low native forb diversity, especially in managed grasslands and pastures where maintaining native forb diversity is a lower priority than maintaining high grass productivity.     

Mayweed chamomile (Anthemis cotula L.) biology and management—A review of an emerging global invader

The globally invasive weed, mayweed chamomile (Anthemis cotula L.) is an annual, bushy, ill-scented herb, originating in Eurasia. It is aggressively weedy in croplands, field-side ditches, wet areas and along roadsides, especially in slightly acidic, nitrogen-rich, clay-loam soils. In addition to interfering with crop growth, the weed causes dermatitis and eye irritation in humans, skin rashes and sour mouth in domesticated mammals, and off-flavours in cow's milk through forage contamination. Although A. cotula may be managed effectively with some broadleaf herbicides in cereal crops, it is much more difficult to manage in broadleaved crops and cover crops. In some regions, aggressive use of relatively few herbicides has selected for acetolactate synthase herbicide resistance in A. cotula. Therefore, A. cotula poses serious ecological and economic challenges in many regions. Despite this threat, the details of A. cotula biology and ecology in the context of environmental change remain relatively unknown. For example, the reason for the invasiveness of A. cotula remains uncertain, but is presumed to be due to abundant seed production, allelochemicals, mycorrhizal associations, minimal herbivory in invaded ranges, ability to attract generalist pollinators through an extended flowering period and adaptive capacity in a wide range of soil types and conditions. In this paper, we comprehensively review the literature and ongoing work on A. cotula and provide a research agenda to improve understanding and management of this species.     

The influence of the soil management systems on aboveground and seed bank weed communities in olive orchards

The biodiversity of farmed landscapes is, in the context of agricultural intensification, a key aspect with regard to improving the sustainability of agroecosystems. Olive groves are undergoing rapid changes because of the spread of intensive farming systems, which may have negative environmental impacts. This paper reports a survey on the aboveground flora and seed banks in five olive groves located in Andalusia (Southern Spain). In this study, the following three management systems have been compared: no‐tillage, with the mowing of spontaneous weedy vegetation; no‐tillage, with the mowing of planted cover crops (Poaceae); and conventional tillage practices. Results showed that coverage and an abundance of vegetation are favored by spontaneous weedy vegetation with mowing management, while the richness of aboveground species was affected by landscape diversity and the presence of edges, which increases the richness and diversity of aboveground flora species in olive groves. Seed bank composition showed a low relationship with aboveground flora in the three cover crop management systems. The multivariate analysis performed pointed to those seed species that have a major influence on the aboveground flora communities of each of the three agricultural systems. The seed bank was clearly impoverished in terms of both abundance and species richness after the long‐term conventional tillage practices. We conclude that the intensive long‐term conventional tillage dramatically reduces weed communities in olive orchards and the subsequent ecosystem services provided by them.