Global change and associated abiotic stresses, such as drought and heat waves, are increasingly predisposing forest trees to fungal pathogens. Many of these pathogens persist in a latent state within their hosts, hindering early detection and limiting accurate assessments of their current distribution. The fungus Cryptostroma corticale, the causal agent of the Sooty Bark Disease (SBD) on maple trees, is one such organism: it can remain latent within the host then become pathogenic and sporulate under abiotic stress. The fungus then colonises weakened trees, leading to dieback and mortality. Despite its emergence across Europe and the North American West Coast, there is a lack of knowledge about its latent distribution within host trees and the reliability of diagnostic approaches. In this study, we investigated the presence of C. corticale within healthy-looking sycamore maples, sampling at different tree heights and depths. During sampling, we observed numerous stains within the vascular tissues which were associated with the presence of C. corticale, particularly in the lower trunk, even though stains were more frequently observed in branches. Greenish stains were strongly correlated with fungal detection. The pathogen was predominantly detected at the collar and at 1.30-m height, suggesting that sampling at 1.30 m is a reliable proxy for rapid assessment without felling the tree. Our findings indicate that latent infections are widespread, since almost all sampled healthy-looking trees tested positive for the pathogen. This work shows that latent presence of C. corticale within infected maple stands is high and could potentially trigger severe outbreaks under abiotic stress conditions. An efficient survey method based on sampling the outer 1 cm of wood and bark from the trunk at 1.30 m above ground would improve monitoring and management of this emerging pathogen.

Despite the strong legal framework provided by the European Union (EU) Plant Health Regulation, its implementation by Member States remains constrained by gaps in biological and epidemiological knowledge, as well as by insufficient information for the reliable diagnosis of several quarantine pathogens. By outlining these challenges, we identify scientific needs and promising avenues for improvement, providing guidance to strengthen early detection, risk-based surveillance, and diagnostic reliability across the EU.

Hymenoscyphus fraxineus is an invasive forest fungal pathogen that induces severe dieback in European ash populations. The spread of the disease has been closely monitored in France by the forest health survey system which has made it possible to record the symptoms observed in the plots visited. We have developed a mechanistic-statistical model using a partial differential equation (PDE) that describes the spread of the disease. It is particularly adapted for pathogen population dynamics driven by propagation of airborn spores and it allows us to take into account climate (summer temperature and spring rainfall), Allee effect induced by limited sexual partner encounters and host density. We fitted this model using available disease reports. We estimated the parameters of our model by a bayesian method, first identifying the appropriate ranges for the parameters, which led to a model reduction, and then using an adaptive multiple importance sampling algorithm for fitting. The model reproduces well the propagation observed in France over the last 20 years. In particular, it predicts the absence of disease impact in the south east of the country and its weak development in the Garonne valley in south-west France. Summer temperature is the factor with the highest overall effect on disease spread and explains its limited impact in southern France. However, the Allee effect and the heterogeneity of spring precipitation did not have a significant impact on the expansion of H. fraxineus across France and could be disregarded for this large-scale modeling. The model can be used to infer the average annual dispersal of H. fraxineus in France.

Mycoviruses, viruses infecting fungi, have been identified in several ascomycetes as single infections or mixed infections. These interactions with plant pathogenic fungi have been associated with hyper- or hypovirulence. This report focuses on single and mixed mycovirus infection of the plant pathogenic fungus Cryptostroma corticale, the causal agent of sooty bark disease (SBD) affecting maple trees in Europe and North America. In humans, exposure of C. corticale spores causes maple bark disease (MBD), causing hypersensitive pneumonitis and allergic asthma with viral-like symptoms. In this study, we identified four species of single-stranded, positive-sense (ss+) RNA mycoviruses that are phylogenetically diverse, including one Mitovirus: Cryptostroma corticale mitovirus 1 (CcMV1) and three Narnavirus species: Cryptostroma corticale narnavirus 1, 2, and 3 (CcNV1, 2, and 3). Notably, CcMV1 shows predicted secondary structures in both 5' and 3' UTRs, while CcNV1 and CcNV3 exhibited strong secondary structures at the 3' UTR. These four mycoviruses were prevalent in 45% (n = 35) of the isolates tested, and growth assays of single infection and the most complex mixed infection showed faster radial expansion compared to a virus-free isolate. These findings reveal single and mixed mycoviruses infections in C. corticale differentially affecting fungal growth, with potential implications for SBD pathogenesis and human MBD risk.

Temperate forests are facing increasing threats due to climate change, affecting their functionality and ecological services. While long-term climate impacts on tree mortality have been extensively studied, the role of extreme events, especially cold, remains understudied. We analysed mortality in 19,056 silver fir and Norway spruce trees throughout France between 2018 and 2023. We created mortality models based on tree and stand characteristics, and included extreme climatic events variables related to drought, heat and cold, and their frequency, intensity and duration. Models showed an area under the curve (AUC) of 0.83 for silver fir and 0.81 for Norway spruce, with extreme climatic events explaining 70 % and 29 % of mortality for silver fir and Norway spruce, respectively. Extreme cold was a major driver of tree mortality in both species, accounting for 33 % of mortality in silver fir and 5.3 % in Norway spruce. For both species, the effect exceeded that of heat (8.7 % and 4.4 % for silver fir and Norway spruce, respectively) and of drought for fir (28.5 % and 18.9 % for silver fir and Norway spruce, respectively). Surprisingly, most cold extremes had a positive effect on tree vitality, thereby reducing mortality. This beneficial effect of frost likely reflects decreased pathogen activity, strongly regulated by autumn and winter temperatures. However, season-specific analyses revealed contrasting responses for silver fir: extreme cold events occurring in autumn exerted a stronger positive influence that outweighed the negative effect of extreme winter cold, which increased mortality likely due to the species’ high sensitivity to severe frost. These beneficial effects of cold are likely already diminishing under ongoing warming and may continue to decline, potentially increasing species’ vulnerability. Overall, our findings highlight the significant—and complex—role of extreme cold events, with effects varying across seasons and species, emphasizing its integration into forest vulnerability assessments.

Ash dieback, induced by Hymenoscyphus fraxineus, a pathogenic ascomycete native to East Asia, has severely affected ash stands in Europe, raising questions about the future of the species. Reports on the relationship between host density and disease incidence are contradictory. Although the most recent studies indicate a reduction in disease severity at lower host densities, the evidence remains largely correlative, with the only study experimentally manipulating host density concluding that no effect of host density on ash dieback can be demonstrated. We investigated the impact of host density and tree species mix on the evolution of ash dieback and subsequent radial growth of affected trees. Data were extracted from a network of permanent thinning trials comprising pure and mixed stands of even-aged ash and a progeny trial where ash dieback was monitored from 2010 to 2015 (39 plots at seven sites). We showed that host density, estimated from ash basal area, has a significant impact on the evolution of ash dieback and subsequent growth of affected stands. Large ash trees at low densities suffered little from the disease. The impact on ash growth is mainly due to the reduction in disease severity, although a significant effect of tree species mixing on ash growth also occurs for healthy trees. As ash trees are often present at low densities in mixtures, this should mitigate ash dieback.

Sexual to asexual transition is described as a process whereby asexual lineages emerge within sexual species. This phenomenon gives rise to many questions about the maintenance of sexual reproduction and the evolution of asexuality in these organisms. The poplar rust fungus Melampsora larici-populina has a complex life cycle, which is typical of rust fungi (Pucciniales). It alternates between a sexual reproduction phase on larch trees ( Larix spp.) and rounds of asexual multiplication on poplar trees ( Populus spp.). This alternation between sexual and asexual reproduction shows some similarities with the cyclical parthenogenesis observed in aphids and daphnia. This study challenges the classic understanding of the M. larici-populina life cycle. Our results demonstrate the existence of many distinct lineages that reproduce asexually through the years, skipping the sexual phase. We conducted a comprehensive population genetic analysis, utilizing 21 microsatellite markers and data from over 2000 individuals gathered over an extended period of time from various locations in France. A clustering analysis identified a group of multilocus lineages that displayed all hallmarks of the genetic consequences of asexual reproduction, including highly negative and large variance among loci of the inbreeding coefficient ( F IS). This indirect evidence for asexual reproduction was confirmed by the direct observation of these asexual lineages being repeatedly sampled over the years, confirming the findings of variations in M. larici-populina life cycle with lineages that bypass the mandatory sexual phase. While sexual lineages are predominant throughout France, asexual lineages are more prevalent in the south of the country, due to possible environmental or ecological factors that allow the overwintering of asexual forms. The discovery of variations in the life cycle in this species offers insights into the evolution from sexual to asexual reproduction encountered in many pathogen species. It could serve as a model organism for studying the transition from sexual to asexual reproductive mode. ### Competing Interest Statement The authors have declared no competing interest.

Increasingly frequent drought events can favour forest disease emergence. Sooty bark disease (SBD) of Acer pseudoplatanus (sycamore maple) is a good example of this phenomenon. Records of its causal agent, Cryptostroma corticale, invasive in Europe, have increased since the 2000s in central and southern Europe. The pathogen is found asymptomatically in host tissues and switches to a pathogenic lifestyle following abiotic stress. This latent phase hinders the pathogen's early detection. In this study, we assessed the prevalence of C. corticale in asymptomatic trees in France. Our study covered six regions, each including a city and its nearby peri-urban and forested ecosystems, representing a human gradient of influence. We assessed the pathogen's presence in 540 wood samples from asymptomatic maple trees by using real-time PCR. The prevalence was 13.6%, across all plots. The pathogen appears to be widespread in the natural sycamore maple stands of France, increasing the risk of disease development following future drought events. Host density and 3-year accumulated water deficit best explained detection of C. corticale in asymptomatic sycamore maples. However, the detection of the fungus was not related to the level of human influence, as no significant differences were observed along the urban-to-forest gradient. Furthermore, C. corticale was detected in asymptomatic hosts even in regions with limited reports of SBD, indicating that the local reporting frequency of the disease does not reflect the latent presence of the pathogen.

Hymenoscyphus fraxineus causes ash dieback in Europe. It overwinters on ash leaf residue (rachis) within the forest litter. In late spring, the fungus produces apothecia on the rachises and releases ascospores to infect leaves. Previous studies reported that H. fraxineus was able to produce apothecia on the rachis for 5 years after the leaf infection under artificial conditions. However, ash litter is known to decompose rapidly in situ. We therefore monitored the decomposition kinetics of ash leaf debris and the persistence of the pathogen, as well as its ability to produce apothecia in the forest litter. For this, leaves shed in autumn in stands affected by ash dieback were placed in mesh bags and left in the forest litter for 6, 18 and 30 months. At each sampling period, litter mass loss and level of colonization of the rachises by H. fraxineus were measured, as was the pathogen's ability to produce apothecia on them. Despite high fragmentation, about 14% of the rachis dry weight remained in the mesh bags after 30 months, and the pathogen retained the ability to produce apothecia on these rachises. A simulation estimating the age composition of the colonized rachises present in the litter during the fruiting period was developed from these results. It shows that the persistence of H. fraxineus in old rachises of the litter represents a reservoir of inoculum that could compensate for poor colonization of autumn leaves and revive local outbreaks after years of unfavourable weather for the development of the pathogen.

Climate shapes the distribution of plant-associated microbes such as mycorrhizal and endophytic fungi. However, the role of climate in plant pathogen community assembly is less understood. Here, we explored the role of climate in the assembly of Phytophthora communities at >250 sites along a latitudinal gradient from Spain to northern Sweden and an altitudinal gradient from the Spanish Pyrenees to lowland areas. Communities were detected by ITS sequencing of river filtrates. Mediation analysis supported the role of climate in the biogeography of Phytophthora and ruled out other environmental factors such as geography or tree diversity. Comparisons of functional and species diversity showed that environmental filtering dominated over competitive exclusion in Europe. Temperature and precipitation acted as environmental filters at different extremes of the gradients. In northern regions, winter temperatures acted as an environmental filter on Phytophthora community assembly, selecting species adapted to survive low minimum temperatures. In southern latitudes, a hot dry climate was the main environmental filter, resulting in communities dominated by drought-tolerant Phytophthora species with thick oospore walls, a high optimum temperature for growth, and a high maximum temperature limit for growth. By taking a community ecology approach, we show that the establishment of Phytophthora plant pathogens in Europe is mainly restricted by cold temperatures.

Key message Presence of Phytophthora ramorum (Werres, De Cock, and Man in ‘t Veld ) in western France was studied after the detection of this invasive pathogen in 2017 in Larix kaempferi (Lamb.) and eradication of the affected stands. P. ramorum was seldom detected in the area of the outbreak in the year following eradication. However, we confirm that P. ramorum can multiply to epidemic level on chestnuts ( Castanea sativa Mill.) in the absence of larch ( Larix spp.). This represents the major risk in France. Context Phytophthora ramorum is an invasive oomycete that causes significant damage in the USA and Europe. Although the pathogen has been present in nurseries in France since 2002, the first outbreaks in forest stands were identified in 2017 in plantations of Larix kaempferi in two forests in western France (Saint-Cadou and Hanvec). In order to limit the development of the epidemic, neighboring larch stands were clear-cut. Aim This study investigated the presence of P. ramorum in the affected area after the eradication treatment. Methods Larch stands located within a 18-km radius of the reported outbreaks were investigated. We also monitored the native woody hosts present in infected clear-cut larch stands and in the vicinity of seven ornamental nurseries that had been infected by P. ramorum on several occasions in the past. Results Overall, a very limited presence of P. ramorum was detected in 2018–2021. Two new stands of infected L. kaempferi were found close to the main initial outbreak, in Saint-Cadou and Saint-Rivoal. The pathogen was only detected on rhododendrons and chestnut trees (Castanea sativa Mill.) in the vicinity of the outbreaks. In the Saint-Cadou state Forest, an outbreak of the disease developed in 2019–2021 on chestnut trees even though all the mature larch trees had been felled. P. ramorum was also detected near two of the formerly infected ornamental nurseries, on Castanea sativa and on rhododendrons. Conclusion While larches and rhododendrons are uncommon in the forests of north-western France, chestnut trees are present in 21–25% of the forest and therefore represent the major risk for the survival of P. ramorum in the region.

The globalization in plant material trading has caused the emergence of invasive pests in many ecosystems, such as the alder pathogen Phytophthora ×alni in European riparian forests. Due to the ecological importance of alder to the functioning of rivers and the increasing incidence of P. ×alni-induced alder decline, effective and accessible decision tools are required to help managers and stakeholders control the disease. This study proposes a Bayesian belief network methodology to integrate diverse information on the factors affecting the survival and infection ability of P. ×alni in riparian habitats to help predict and manage disease incidence. The resulting Alder Decline Network (ADnet) management tool integrates information about alder decline from scientific literature, expert knowledge and empirical data. Expert knowledge was gathered through elicitation techniques that included 19 experts from 12 institutions and 8 countries. An original dataset was created covering 1189 European locations, from which P. ×alni occurrence was modeled based on bioclimatic variables. ADnet uncertainty was evaluated through its sensitivity to changes in states and three scenario analyses. The ADnet tool indicated that mild temperatures and high precipitation are key factors favoring pathogen survival. Flood timing, water velocity, and soil type have the strongest influence on disease incidence. ADnet can support ecosystem management decisions and knowledge transfer to address P. ×alni-induced alder decline at local or regional levels across Europe. Management actions such as avoiding the planting of potentially infected trees or removing man-made structures that increase the flooding period in disease-affected sites could decrease the incidence of alder disease in riparian forests and limit its spread. The coverage of the ADnet tool can be expanded by updating data on the pathogen's occurrence, particularly from its distributional limits. Research on the role of genetic variability in alder susceptibility and pathogen virulence may also help improve future ADnet versions.

Invasive pathogens are a major threat to forest health especially in managed forest with a low diversity of tree species. The dieback of Fraxinus spp. caused by the fungus Hymenoscyphus fraxineus that occurs in Europe is the latest example of pathogen invasion causing widespread damage in forests. Ash dieback severity has been shown to be strongly affected by environment, in particular by stands features such as overall tree density or proportion of ashes. The fact that H. fraxineus reproduce mostly through heterothallic sexual reproduction suggest that an Allee effect could limit the mating success at low host densities, thus limiting inoculum production and disease development. Populations of H. fraxineus were monitored during the vegetation period in a network of stands across a host density gradient in forest and non-forest environment (hedges and small woods). Ash dieback, basal area of ash, density of infected ash leaf debris (rachis) and apothecia in the litter and ascospores load in the air were determined in the different environments during two years. We showed significant differences between forest and non-forest environment with ash dieback, infection rate and inoculum production higher in forest settings. Host density significantly affected disease development, with crown dieback, density of infected rachis in the litter and inoculum production increasing with host density. We also demonstrated that fruiting rate, i.e. the number of apothecia per infected rachis dry weight, is strongly dependent on infected rachis density. Inoculum production is therefore limited at low host densities. Such a component Allee effect could be important in H. fraxineus epidemiology and invasion dynamic.

The sooty bark disease (SBD) is an emerging disease affecting sycamore maple trees (Acer pseudoplatanus) in Europe. Cryptostroma corticale, the causal agent, putatively native to eastern North America, can be also pathogenic for humans causing pneumonitis. It was first detected in 1945 in Europe, with markedly increasing reports since 2000. Pathogen development appears to be linked to heat waves and drought episodes. Here, we analyse the conditions of the SBD emergence in Europe based on a three-decadal time-series data set. We also assess the suitability of aerobiological samples using a species-specific quantitative PCR assay to inform the epidemiology of C. corticale, through a regional study in France comparing two-year aerobiological and epidemiological data, and a continental study including 12 air samplers from six countries (Czechia, France, Italy, Portugal, Sweden and Switzerland). We found that an accumulated water deficit in spring and summer lower than -132 mm correlates with SBD outbreaks. Our results suggest that C. corticale is an efficient airborne pathogen which can disperse its conidia as far as 310 km from the site of the closest disease outbreak. Aerobiology of C. corticale followed the SBD distribution in Europe. Pathogen detection was high in countries within the host native area and with longer disease presence, such as France, Switzerland and Czech Republic, and sporadic in Italy, where the pathogen was reported just once. The pathogen was absent in samples from Portugal and Sweden, where the disease has not been reported yet. We conclude that aerobiological surveillance can inform the spatial distribution of the SBD, and contribute to early detection in pathogen-free countries.

Les changements globaux, combinant réchauffement climatique et invasions biologiques, menacent de plus en plus les écosystèmes forestiers. Différentes essences forestières ont été victimes de crises sanitaires ces dernières années en Europe. Les agents biotiques (champignons pathogènes, insectes ravageurs, bactéries, nématodes,…) peuvent jouer différents rôles dans ces crises, que ce soit en tant que facteurs prédisposants, déclenchants (primaires) ou aggravants (secondaires) selon le concept de Manion (1981). À la lumière des crises passées et actuelles impliquant des agents biotiques, nous passons en revue les outils et mesures de gestion disponibles afin de prévenir, éradiquer, enrayer ces crises sanitaires ou alors limiter leur impact. Messages clésLes changements climatiques menacent les écosystèmes forestiers.Les agents biotiques jouent souvent un rôle déclenchant ou aggravant dans les crises sanitaires.Des mesures de gestion peuvent être prises pour limiter l'impact des crises sinitaires.

When a non-native species succeeds in establishing in a new habitat, one of the possible responses is to attempt its eradication. In the present study, we analysed European eradication programmes against non-native pests and pathogens of woody plants (PPWP) from 1945 to date. Our main goal was to identify which factors affect the success of an eradication programme, reinforcing guidelines for future eradication of PPWP. Data on eradication campaigns were obtained from online databases, scientific and grey literature, and Plant Protection Organizations’ reports. Factors influencing eradication success for both arthropods and pathogens were analysed with LASSO regression and decision tree learning. A total of 848 cases officially declared as eradication attempts were documented in our database (8-fold higher than previous reports). Both the number of programmes and their rate of success increased sharply over the last two decades. Only less than 10% of the non-native organisms affecting woody plants were targeted for attempted eradication despite the high economic and ecological impacts caused by some species for which no efforts were undertaken. Almost one-third of the officially declared cases of eradication concerned organisms that were still restricted to the material with which they were introduced. For these cases the success rate was 100%. The success rate of established species was only 50% for arthropods and 61% for pathogens. The spatial extent of the outbreak was the factor that most affected the outcome of eradication campaigns. The eradication success decreased abruptly above 100 ha for arthropods and 10 ha for pathogens. Additionally, other variables were shown to influence the outcome of eradication programmes, in particular the type of environment, with the highest eradication success rate found in nurseries and glasshouses, with successful outcomes increasing if quarantine measures were applied and when monitoring included asymptomatic plants. Particular species traits may reduce eradication success: parthenogenetic arthropods, saprotrophic pathogens, wind dispersal, the possibility to remain asymptomatic indefinitely, and the existence of resting spores or stages. In conclusion, small affected areas, quick response, and efficient implementation of quarantine restrictions, together with particular species traits, may allow a high probability of eradication success. Preparedness at the country and European level would allow a larger number of target species to be included in future eradication programmes.

Dothistroma needle blight (DNB) is an important disease of Pinus species that can be caused by one of two distinct but closely related pathogens; Dothistroma septosporum and Dothistroma pini. Dothistroma septosporum has a wide geographic distribution and is relatively well-known. In contrast, D. pini is known only from the United States and Europe, and there is a distinct lack of knowledge regarding its population structure and genetic diversity. The recent development of 16 microsatellite markers for D. pini provided an opportunity to investigate the diversity, structure, and mode of reproduction for populations collected over a period of 12 years, on eight different hosts in Europe. In total, 345 isolates from Belgium, the Czech Republic, France, Hungary, Romania, Western Russia, Serbia, Slovakia, Slovenia, Spain, Switzerland, and Ukraine were screened using microsatellite and species-specific mating type markers. A total of 109 unique multilocus haplotypes were identified and structure analyses suggested that the populations are influenced by location rather than host species. Populations from France and Spain displayed the highest levels of genetic diversity followed by the population in Ukraine. Both mating types were detected in most countries, with the exception of Hungary, Russia and Slovenia. Evidence for sexual recombination was supported only in the population from Spain. The observed population structure and several shared haplotypes between non-bordering countries provides good evidence that the movement of D. pini in Europe has been strongly influenced by human activity in Europe.

Ash dieback, induced by an invasive ascomycete, Hymenoscyphus fraxineus, has emerged in the late 1990s as a severe disease threatening ash populations in Europe. Future prospects for ash are improved by the existence of individuals with natural genetic resistance or tolerance to the disease and by limited disease impact in many environmental conditions where ash is common. Nevertheless, it was suggested that, even in those conditions, ash trees are infected and enable pathogen transmission. We studied the influence of climate and local environment on the ability of H. fraxineus to infect, be transmitted and cause damage on its host. We showed that healthy carriers, i.e. individuals showing no dieback but carrying H. fraxineus, exist and may play a significant role in ash dieback epidemiology. The environment strongly influenced H. fraxineus with different parameters being important depending on the life cycle stage. The ability of H. fraxineus to establish on ash leaves and to reproduce on the leaf debris in the litter (rachises) mainly depended on total precipitation in July-August and was not influenced by local tree cover. By contrast, damage to the host, and in particular shoot mortality was significantly reduced by high summer temperature in July-August and by high autumn average temperature. As a consequence, in many situations, ash trees are infected and enable H. fraxineus transmission while showing limited or even no damage. We also observed a decreasing trend of severity (leaf necrosis and shoot mortality probability) with the time of disease presence in a plot that could be significant for the future of ash dieback.

Ash dieback in Europe is caused by an invasive alien pathogen originating from East Asia, the helotialean ascomycete fungus Hymenoscyphus fraxineus. This disease first emerged in the early 1990s in North-Eastern Poland, and the pathogen successively invaded most of Europe, in total 32 countries, in the next decades, causing substantial damage and mortality of the highly susceptible Fraxinus excelsior and Fraxinus angustifolia, while the third European ash species, Fraxinus ornus, is not affected. In this chapter, we review the general characteristics of the disease, in particular its disease cycle, and the perspectives that tolerance to H. fraxineus in the populations of ash may lead to remission of ash dieback over time through natural selection and accelerated by breeding. Likewise, an updated view of the possible long-term ecological impact of ash dieback is presented with a review of the role of stand, site, and environmental factors in the epidemiology of the disease. While disease intensity is generally favored by high moisture levels (soil humidity and precipitation), the sensitivity of H. fraxineus to high summer temperatures constrains the impact of ash dieback in Southern Europe. Likewise, the impact of the disease is often lower on ash trees that occur isolated or at low frequency (solitary trees in the open landscape or in hedges and mixed forest stands with low proportion of ash) compared to trees in ash-dominated forest stands. Finally, we discuss the role of the microbiota associated with ash and of H. fraxineus mycoviruses in relation to ash dieback.