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.     

Evidence of sedimentation inequality along riparian areas colonised by Impatiens glandulifera (Himalayan balsam)

Soil loss from riparian areas supporting the annual invasive weed, Impatiens glandulifera (Himalayan balsam), was measured and compared with equivalent values recorded at nearby, topographically similar areas supporting perennial vegetation over a cumulative seven-year period, along sections of two separate river systems; one in Switzerland, and one in the UK. Soil loss from colonised locations was significantly greater than from reference locations in four of the seven measurement periods. Despite contrasting results, standard deviations, based on soil losses and gains, were predominantly higher for colonised areas at both rivers over most monitoring periods. These findings indicated that areas colonised by Himalayan balsam experience higher sediment flux in comparison with areas free of invasion. Here, we test those original interpretations by reinterrogating the datasets using a more robust analysis of inequality. Nine datasets were tested, five of which (i.e. 56%) showed that sediment flux was significantly greater at Himalayan balsam-invaded areas than at reference areas. Three datasets showed no difference in sediment flux between invaded and reference areas (33%), and one (11%) showed higher sediment flux at reference areas. Most results uphold our original interpretations and support our hypothesis that hydrochory probably dictates where colonisation initially occurs, by depositing Himalayan balsam seeds in slack or depressional areas along river margins. Once Himalayan balsam becomes established and sufficient perennial vegetation is displaced, seasonal die-off and depleted vegetation cover may increase the risk that some areas will experience significantly higher sediment flux.     

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.     

Host specificity testing and assessment of the pathogenicity of the rust, Puccinia abrupta var. partheniicola, as a biological control agent of Parthenium weed (Parthenium hysterophorus)

Parthenium hysterophorus, a native of Central America, is a problem weed of Australian rangeland, particularly in Queensland. Following field surveys in Mexico, the rust fungus Puccinia abrupta var. partheniicola was selected as a potential biological control agent. One isolate was chosen for further investigation after infection studies with one Kenyan and five Mexican isolates. Assessment of inoculation conditions showed that temperatures of less than 20° C and dew periods of more than 6 hours were required for abundant pustule production. Infection with the rust hastened leaf senescence, significantly decreased the life span and dry weight of Parthenium plants, and reduced flower production 10-fold. Subsequent host-range studies against 120 species and varieties, with further screening against a limited number of species conducted under a range of environmental regimes, indicated the rust to be sufficiently host-specific to be considered for introduction. Additional host-range tests against sunflowers demonstrated that resistance to P. abrupta var. partheniicola was not modified by prior inoculation with P. helianthi.     

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.     

Host range of Puccinia expansa Link (=P. glomerata Grev.), a possible fungal biocontrol agent against Senecio weeds

Nineteen species of the genus Senecio, 18 species of cultivated Compositae and seven of the most common crop plants were tested in the glasshouse for susceptibility to Puccinia expansa Link (=P. glomerata Grev.), collected from Senecio alpinus (L.) Scop. in Switzerland. In the genus Senecio certain species groups only were attacked. Within these species groups the degree of infection of the different species was similar. All collections of the problem weeds S. alpinus and S. jacobaea L. were severely attacked whereas only one collection of S. vulgaris L. was slightly infected. Two cultivars of S. cineraria DC., an ornamental plant, were slightly susceptible if inoculated at the stage of two to four fully developed leaves. Older plants were not attacked. The low teliospore germination of P. expansa (6%) could be increased by storing the spores for 21 days on water agar at 2° or 8°C under continuous darkness, after which 30 and 70% germination could be obtained. These results show that P. expanses is specialized enough to be used in biocontrol of S. alpinus and S. jacobaea. La gamme des hôtes de Puccinia expansa Link (= P. glomerata Grev.), champignon éventuellement utilisable dans la lutte biologique contre Senecio spp. Dix-neuf espèces du genre Senecio, 18 Composées cultivées et sept espèces des cultures les plus répandues ont subi en serre des épreuves de sensibilité envers Puccinia expansa Link (=P. glomerata Grev.), récoltée sur Senceio alpinus (L.) Scop. en Suisse. Dans le genre Senecio, seuls certains groupes d'espèces ont été attaqués. A l'intérieur de ces groupes, le niveau d'infection était semblable chez les différentes espèces. Toutes les collections de S. alpinus et S. jacobaea L., espèces adventices difficiles à maîtriser, ont subi des attaques sévères tandis qu'une seule collection de S. vulgaris L. a fait preuve d'une infection légère. Deux variétés de S. cineraria DC., plante d'ornement, se sont montrées légèrement sensibles lorsque l'inoculation a eu lieu au stade deux à quatre feuilles en plein développement. Les plantes plus mûres n'ont pas subi d'attaque. La faible germination des téliospores de P. expansa (6%) s'est améliorée après stockage des spores pendant 21 jours sur de la gélose à 2 ou 8 Cen obscurité permanente; alors une germination de 30 et 70% a été réalisée. Ces résultats font voir que P. expansa est suffisamment spécifique pour servir dans la lutte biologique contre S. alpinus et S. jacobaea. Das Wirtsspektrum von Puccinia expansa Link (=P. glomerata Grev), eines möglicherweise zur Bekämpfung von Unkräutern aus der Gattung Senecio geeigneten Pilzes Neunzehn Arten der Gattung Senecio, 18 Arten kukivierter Compositen und 7 der verbreitetsten Kulturpflanzen wurden im Gewäehshaus auf ihre Anfälligkeit gegenüber Puccinia expansa Link (=P. glomerata Grev.) gepiüft. Der für die Versuche verwendete Pilzstamm wurde in der Schweiz von befallenen Senecio alpinus (L.) Scop. isoliert. In der Gattung Senecio erwiesen sich nur gewisse Artengruppen als anfällig. Innerhalb dieser Gruppen war der Infektionsgrad bei den einzelnen Arten ähnlieh. Alle Sammelmuster der Problemunkräuter S. alpinus und S. jacohaea L. wurden stark befallen, während nur ein Muster von S. vulgaris L. leicht infiziert wurde. Zwei Sorten von S. cineraria DC, cincr Zierpflanze, zeigten sich leicht anfällig, wenn sie im Stadium von 2–4 voll ausgebildeten Blättern infiziert worden waren. Aeltere Ptlanzen wurden nicht befallen. Die niedrige Keimungsrate (6%) der Teliosporen von P. expansa konnte durch Lagerung auf Wasseragar bei 2 oder 8°C während 21 Tagen in dauernder Dunkelheit auf 30 und 70% gesteigert werden. Diese Resultate zeigen, dass P. expansa einen genügend hohen Spezialisationsgrad aufweist, dass ein Einsatz zur biologischen Konrolle von S. alpinus und S. jacobaea möglich erscheint.     

Gastrophysa atrocyanae (Col: Chrysomelidae), an agent for biological control of the dock,Rumex japonicus (Polygonaceae) in China

Abstract

The biology and host specificity of the beetle, Gastrophysa atrocyanea Motch were studied in the laboratory in Nanchang, China. This univoltine insect completed its immature stage in 32–39 days with adult overwintering in soil. A total of 35 plant species from 21 families were tested. Both larvae and adults attacked Rumex japonicus and Rumex acetosa with R. japonicus the main host. Larvae also attacked two Polygonum species, P. hydropiper and P. perfoliatum. But the adults are not concurrent with the two Polygonum species. Though oviposition occurred on five other plant species, none of them supported larval development. Field observations showed that G. atrocyanae caused a progressive decline in natural R. japonicus populations. Thus it is recommended as a valuable biological agent for this weed.     

Low pathotype diversity in a recombinant Puccinia striiformis population through convergent selection at the eastern Himalayan centre of diversity (Nepal)

Worldwide Puccinia striiformis f. sp. tritici (Pst) epidemics have been reported to be driven by few genetic lineages, while a high diversity is evident at the Pst Himalayan centre of diversity. This study investigated the relationship between pathotype diversity and genetic structure in Nepal, the eastern Himalayan region, which has been largely unexplored. Despite the high genetic diversity and recombinant structure detected through microsatellite genotyping, characterization of virulence phenotypes for 62 isolates identified only eight pathotypes, with two pathotypes predominant over all the populations. This is in contrast to the Pakistani and Chinese recombinant populations, where high pathotype diversity is associated with genetic diversity. The most prevalent Nepali pathotype was not a unique clonal lineage, but was represented by seven multilocus genotypes from four distinct genetic subgroups, suggesting strong directional selection on virulence genes, resulting in convergent pathotypes in distinct genetic groups. This convergent selection is discussed in comparison with clonal French and recombinant Pakistani populations. Additionally, the Nepali Pst population carried virulence to 17 out of 24 tested yellow rust resistance genes (Yr), with the absence of virulence to Victo and Early Premium and resistance genes Yr5, Yr10, Yr15, Yr24 and Yr26. Virulence to Yr2, Yr7, Yr27 and YrSu were fixed in all isolates, in line with the deployment of these resistance genes in Nepal. The results reflect the influence of resistance gene deployment on selection of virulence and pathotypes in a recombinant pathogen population, which must be considered in the context of durable resistance gene deployment.     

Wintering of the biotrophic fungus Puccinia lagenophorae within the annual plant Senecio vulgaris: implications for biological weed control

Epidemics of the obligate biotrophic fungus Puccinia lagenophorae might be used to control populations of the annual plant, groundsel, Senecio vulgaris . Insight into the mechanisms of survival of P. lagenophorae over winter may help to explain the number of inoculum sources, and their strength (assessed by number and size of pustules), present in an S. vulgaris population in spring, indicating the probability and rate of progress of a subsequent epidemic. Results of the study indicated survival of the rust as mycelium within the host over winter. Survival outside the host is unlikely, because aecidiospores lost their capacity to germinate over winter and teliospores have not been reported to be infectious. Survival of S. vulgaris plants over winter was reduced by rust infection in autumn. The mortality of S. vulgaris was 30–100% depending on the date of infection. All plants infected early in autumn died but those infected late in autumn were more likely to survive. In turn, poor survival of the host impacted on the survival of P. lagenophorae over winter. Consequently, the results of the study suggest that no inoculum sources, or only a few weak ones, are present in vulgaris populations in spring. This suggestion was supported by observations of an S. vulgaris population at a ruderal site. Therefore, research on biological weed control should focus on increasing the negative impact of P. lagenophorae on S. vulgaris populations while augmenting the probability of survival of the rust over winter to start new epidemics in spring.     

Effect of biological seed treatment withCylindrocarpon olidum var.olidum on control of common bunt (Tilletia laevis) of wheat

The goals of the present study were to determine ifCylindrocarpon olidum var.olidum exerts antibiotic activity on teliospore germination ofTilletia laevis in vitro and to evaluate the efficacy of a seed treatment with this antagonist against artificial seedborne infection in the field under natural cropping conditions. Germination of bunt teliospores was completely inhibitedin vitro on water agar medium supplemented with the antagonist’s culture filtrate. In field experiments seed application reduced the incidence of common bunt from 82.9% to 40.4%, and from 81.4% to 42.0% in 1995/1996 and 1997/1998, respectively.C. olidum var.olidum may have a potential againstT. laevis and is worthy of further research on its use as a biocontrol agent for common bunt. http://www.phytoparasitica.org posting July 14, 2005.     

Altica cyanea (Col: Chrysomelidae) for the biological control of Ludwigia prostrata (Onagraceae) in China

Abstract

Altica cyanea (Weber) damages Ludwigia prostrata Roxb in China. It is multivoltine, having up to six generations a year. The host range of the beetle was examined in the field and in the laboratory, and it was demonstrated that A. cyanea occurs on and attacks the main host L. prostrata and another weed, Rotala indica Koehne. Its ability to damage L. prostrata was studied in field cages in Nanchang. A. cyanea was shown to damage these caged plants heavily and to be a promising biological agent for this weed.     

Economic and financial model to the mass-rearing of Macrolophus pygmaeus (Rambur) (Heteroptera: Miridae), a biological control agent against the tomato moth Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in protected culture

BACKGROUND

Tuta absoluta (Meyrick) is a major pest of tomato produced in glasshouses and open field, causing severe damages to crops, reducing the quality of tomato fruits. The current maintenance of the pest populations below the economic threshold is not achieved by natural and classical control, thus requiring the continuous application of biological control agents (BCAs), under an augmentative or inoculative approach. The present study aims to develop an economic and financial model to evaluate the commercial viability of a continuous mass production of Macrolophus pygmaeus (Rambur), a BCA commonly used against the tomato moth, Tuta absoluta, in protected culture. The estimations for our model were based on two approaches: the farm-level impact analysis and the benefit–cost analysis.

RESULTS

The results of the farm-level analysis show that the adoption of a more sustainable biological control approach is profitable for farmers and the benefit–cost analysis provides evidence that the investment on a new factory dedicated to the mass rearing of M. pygmaeus to control tomato moth populations generates a positive net present value (NPV) of 7.2 million euros, corresponding to an internal rate of return (IRR) of 28.4% per year.

CONCLUSION

Our results are in line with (i) the more recent European Commission proposals for a new Regulation on sustainable use of plant protection products, which includes the reduction of 50% the use and risk of chemical pesticides by 2030 and (ii) most of the existing literature which conclude that new projects on BCA production are worth investments. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.     

Alternaria eichhorniae, a biological control agent for waterhyacinth: mycoherbicidal formulation and physiological and ultrastructural host responses

The bioherbicidal efficacy of different alginate formulations of Alternaria eichhorniae 5 (isolate Ae5), a virulent Egyptian isolate, was compared on waterhyacinth (Eichhornia crassipes). The fungus was formulated as alginate pellets containing mycelium alone, mycelium plus culture filtrate or culture filtrate alone. Each formulation was applied with and without a hydrophilic humectant (Evergreen 500). These formulations were evaluated for disease incidence (DI), and disease severity (DS). Maximum DS, but not DI, was obtained with the alginate pellets of mycelium plus culture filtrate. Alginate formulations supplemented with the hydrophilic polymer were more effective in promoting disease. Physiological changes associated with the treated waterhyacinth plants were determined 3, 6 and 9 days after treatment. Waterhyacinth plants treated with alginate pellets of mycelium plus culture filtrate of Ae5 had the lowest levels of pigments, carbohydrates and relative water content. Infection of waterhyacinth with Ae5 led to a significant increase in total phenols of leaves as compared to control. Penetration of waterhyacinth leaves by the fungus occurred only through the stomata, and the invading hyphae were located in the intercellular spaces of leaf tissues. Cytological changes noted in infected cells included changes in chloroplast, nucleus and mitochondria. Invagination of the plasma membrane, particularly at plasmodesmata was also noticed in infected cells. The associations between the infection process, the physiological disorder and the ultrastructure of infected leaves are discussed.     

Selection of fungal biological control agents of Sclerotium cepivorum for control of white rot by sclerotial degradation in a UK soil

A range of fungal isolates was tested in a three-stage screening system for their ability to degrade sclerotia of Sclerotium cepivorum on agar and in soil, and to reduce white rot disease on onion seedlings. Biological control agents (BCAs) were identified that could degrade up to 60% of sclerotia in soil and significantly reduce white rot disease on onion seedlings. The efficacy of the BCAs was enhanced when applied as wheat bran cultures compared with spore suspensions, and two of the best BCAs from the screening procedures were both identified as Trichoderma viride (L4, S17A). When L4 and S17A were fluid-drilled in guar gum with bulb onion seed in the field white rot symptoms were significantly reduced, but stem base applications applied mid-season had little effect. The strategy of selecting and using BCAs that degrade sclerotia of S. cepivorum and integration with other control methods is discussed.     

Resistance in Australian barley (Hordeum vulgare) germplasm to the exotic pathogen Puccinia striiformis f. sp. hordei,causal agent of stripe rust

Eighty‐eight Australian and 10 international barley cultivars were assessed for resistance to the barley stripe (yellow) rust pathogen, Puccinia striiformis f. sp. hordei (Psh). All cultivars were tested for seedling resistance to two UK‐derived isolates of Psh (11.01 and 83.39) that were shown to differ in virulence based on responses on 16 differential barley genotypes. The 98 barley cultivars differed substantially in stripe rust response; 45% were susceptible to Psh 11.01, 53% to Psh 83.39 and 44% to both isolates. The observed diverse infection types (ITs) suggest the presence of both known and uncharacterized resistance. However, further multipathotype tests are required for accurate gene postulation. The Yerong × Franklin (Y×F) doubled haploid (DH) population was phenotypically assessed as seedlings using both Psh isolates. Yerong and Franklin were immune and highly resistant, respectively, to both isolates used in this study. Marker‐trait and QTL mapping identified a major effect on the long arm of chromosome 7H contributed by Franklin in response to all isolates. The resistance of Yerong was mapped to 113·96 and 169·38 cM on chromosome 5HL in response to Psh 11.01 and 83.39, respectively. The Psh resistance sources identified in this study can be used for further genetic analysis and introgression for varietal improvement.