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Human-altered ecological disturbances may challenge system resilience and disrupt biological legacies maintaining ecosystem recovery. Yet, the extent to which novel regimes challenge these legacies varies. This may be partially explained by differences in the vulnerability of life history strategies to disturbance characteristics. In the fire-prone, resprouter-dominated coast redwood forests of California, the introduced disease sudden oak death (SOD) alters fuel profiles, fire behavior, and aboveground tree mortality; however, this system is dominated by resprouting trees that are well-adapted to aboveground damage, and belowground survival of individuals may represent the principal biological legacy connecting pre- and post-fire communities. Much of the research exploring altered disturbances and forest recovery has focused on legacies determined by seed dispersal and aboveground survival of adults. In this work, we use pre- and post-fire data from a long-term monitoring network to assess the impacts of novel disturbance interactions between wildfire and SOD on the belowground survival and vegetative reproduction of resprouters. We found that increasing accumulation of coarse woody surface fuels from SOD-killed hosts decreased the likelihood of belowground survival for resprouting tanoak trees, but not for redwoods. Tanoaks' belowground survival was negatively related to substrate burn severity, which increased with the volume of surface fuels from hosts, suggesting heat damage as a possible mechanism influencing altered patterns of resprouter mortality. These impacts increased with decreasing tree size. By contrast, redwood and tanoak trees that survived both disturbances resprouted more vigorously, regardless of post-fire infection by P. ramorum, and generated similar recruitment at the stand level. Our results demonstrate that disease-fire interactions can narrow recruitment filters for resprouters, which could impact long-term population and demographic structure; yet, compounded disturbance may also reduce stand density and disease pressure, allowing competitive release of survivors. Resprouters displayed vulnerabilities to altered disturbance, but our research suggests that legacies maintained by resprouting may be more resilient to certain compounded disturbances, compared to seed-obligate species, because of high rates of individual survival under increasingly severe events. These trends have important implications for conservation of declining tree species in SOD-impacted forests, as well as predictions of human impacts in other disturbance-prone systems where resprouters are present., (© 2018 by the Ecological Society of America.)

The first wildfires in sudden oak death-impacted forests occurred in 2008 in the Big Sur region of California, creating the rare opportunity to study the interaction between an invasive forest pathogen and a historically recurring disturbance. To determine whether and how the sudden oak death pathogen, Phytophthora ramorum, survived the wildfires, we completed intensive vegetation-based surveys in forest plots that were known to be infested before the wildfires. We then used 24 plot-based variables as predictors of P. ramorum recovery following the wildfires. The likelihood of recovering P. ramorum from burned plots was lower than in unburned plots both 1 and 2 yr following the fires. Post-fire recovery of P. ramorum in burned plots was positively correlated with the number of pre-fire symptomatic California bay laurel (Umbellularia californica), the key sporulating host for this pathogen, and negatively correlated with post-fire bay laurel mortality levels. Patchy burn patterns that left green, P. ramorum-infected bay laurel amidst the charred landscape may have allowed these trees to serve as inoculum reservoirs that could lead to the infection of newly sprouting vegetation, further highlighting the importance of bay laurel in the sudden oak death disease cycle., (© 2012 The Authors. New Phytologist © 2012 New Phytologist Trust.)

Exotic pathogens and pests threaten ecosystem service, biodiversity, and crop security globally. If an invasive agent can disperse asymptomatically over long distances, multiple spatial and temporal scales interplay, making identification of effective strategies to regulate, monitor, and control disease extremely difficult. The management of outbreaks is also challenged by limited data on the actual area infested and the dynamics of spatial spread, due to financial, technological, or social constraints. We examine principles of landscape epidemiology important in designing policy to prevent or slow invasion by such organisms, and use Phytophthora ramorum, the cause of sudden oak death, to illustrate how shortfalls in their understanding can render management applications inappropriate. This pathogen has invaded forests in coastal California, USA, and an isolated but fast-growing epidemic focus in northern California (Humboldt County) has the potential for extensive spread. The risk of spread is enhanced by the pathogen's generalist nature and survival. Additionally, the extent of cryptic infection is unknown due to limited surveying resources and access to private land. Here, we use an epidemiological model for transmission in heterogeneous landscapes and Bayesian Markov-chain-Monte-Carlo inference to estimate dispersal and life-cycle parameters of P. ramorum and forecast the distribution of infection and speed of the epidemic front in Humboldt County. We assess the viability of management options for containing the pathogen's northern spread and local impacts. Implementing a stand-alone host-free "barrier" had limited efficacy due to long-distance dispersal, but combining curative with preventive treatments ahead of the front reduced local damage and contained spread. While the large size of this focus makes effective control expensive, early synchronous treatment in newly-identified disease foci should be more cost-effective. We show how the successful management of forest ecosystems depends on estimating the spatial scales of invasion and treatment of pathogens and pests with cryptic long-distance dispersal., (© 2012 Filipe et al.)

The transmission ecology of Phytophthora ramorum from bay laurel (Umbellularia californica) leaves was compared between mixed-evergreen and redwood forest types throughout winter and summer disease cycles in central, coastal California. In a preliminary multisite study, we found that abscission rates of infected leaves were higher at mixed-evergreen sites. In addition, final infection counts were slightly higher at mixed-evergreen sites or not significantly different than at redwood sites, in part due to competition from other foliar pathogens at redwood sites. In a subsequent, detailed study of paired sites where P. ramorum was the main foliar pathogen, summer survival of P. ramorum in bay laurel leaves was lower in mixed-evergreen forest due to lower recovery from infected attached leaves and higher abscission rates of infected leaves. Onset of inoculum production and new infections of bay laurel leaves occurred later in mixed-evergreen forest. Mean inoculum levels in rainwater and final infection counts on leaves were higher in redwood forest. Based on these two studies, lower summer survival of reservoir inoculum in bay laurel leaves in mixed-evergreen forest may result in delayed onset of both inoculum production and new infections, leading to slower disease progress in the early rainy season compared with redwood forest. Although final infection counts also will depend on other foliar pathogens and disease history, in sites where P. ramorum is the main foliar pathogen, these transmission patterns suggest higher rates of disease spread in redwood forests during rainy seasons of short or average length.

Sudden oak death (SOD) is an emerging forest disease causing extensive tree mortality in coastal California forests. Recent California wildfires provided an opportunity to test a major assumption underlying discussions of SOD and land management: SOD mortality will increase fire severity. We examined prefire fuels from host species in a forest monitoring plot network in Big Sur, California (USA), to understand the interactions between disease-caused mortality and wildfire severity during the 2008 Basin Complex wildfire. Detailed measurements of standing dead woody stems and downed woody debris 1-2 years prior to the Basin fire provided a rare picture of the increased fuels attributable to SOD mortality. Despite great differences in host fuel abundance, we found no significant difference in burn severity between infested and uninfested plots. Instead, the relationship between SOD and fire reflected the changing nature of the disease impacts over time. Increased SOD mortality contributed to overstory burn severity only in areas where the pathogen had recently invaded. Where longer-term disease establishment allowed dead material to fall and accumulate, increasing log volumes led to increased substrate burn severity. These patterns help inform forest management decisions regarding fire, both in Big Sur and in other areas of California as the pathogen continues to expand throughout coastal forests.

Epidemiological theory predicts that asymmetric transmission, susceptibility, and mortality within a community will drive pathogen and disease dynamics. These epidemiological asymmetries can result in apparent competition, where a highly infectious host reduces the abundance of less infectious or more susceptible members in a community via a shared pathogen. We show that the exotic pathogen Phytophthora ramorum and resulting disease, sudden oak death, cause apparent competition among canopy trees and that transmission differences among canopy trees drives patterns of disease severity in California coast redwood forests. P. ramorum ranges in its ability to infect, sporulate on, and cause mortality of infected hosts. A path analysis showed that the most prolific inoculum producer, California bay laurel (Umbellularia californica), had a greater impact on the mortality rate of tanoak (Lithocarpus densiflorus) than did other inoculum-supporting species. In stands experiencing high tanoak mortality, lack of negative impacts by P. ramorum on bay laurel may increase bay laurel density and subsequently result in positive feedback on pathogen populations. This study demonstrates the degree to which invasive, generalist pathogens can cause rapid changes in forest canopy composition and that differences in transmission can be more important than susceptibility in driving patterns of apparent competition.

In California and Oregon, two recently described oomycete forest pathogens, Phytophthora nemorosa and P. pseudosyringae, overlap in their host and geographic ranges with the virulent P. ramorum, causal agent of "sudden oak death." Epidemiological observations, namely broader geographic distribution and lack of landscape-level mortality, led to the hypothesis they are native to this region, whereas multiple lines of evidence indicate P. ramorum is exotic to North America. We used AFLP analysis to measure genetic variability in the homothallic P. nemorosa and P. pseudosyringae and to evaluate the hypothesis of endemism. We analysed 39 P. nemorosa and 48 P. pseudosyringae isolates (29 American and 19 European) from throughout their geographic and host ranges. In the US, both P. nemorosa and P. pseudosyringae have a dominant AFLP clone with several closely related variants. There is no evidence that genetic diversity is partitioned by host or location in P. nemorosa, but the US P. pseudosyringae clonal lineage is largely nested within a more genetically variable European group. Though the absence of highly variable sampled source populations does not allow us to determine whether each species is native or introduced in the western US with certainty, the results are most consistent with the hypothesis that both are introduced -P. pseudosyringae perhaps from Europe. Invasive Phytophthora species are increasingly being implicated in emergent forest diseases, highlighting the need to identify and characterize both native and previously unknown introduced forest Phytophthoras.

Distinguishing the manner in which dispersal limitation and niche requirements control the spread of invasive pathogens is important for prediction and early detection of disease outbreaks. Here, we use niche modeling augmented by dispersal estimation to examine the degree to which local habitat conditions vs. force of infection predict invasion of Phytophthora ramorum, the causal agent of the emerging infectious tree disease sudden oak death. We sampled 890 field plots for the presence of P. ramorum over a three-year period (2003-2005) across a range of host and abiotic conditions with variable proximities to known infections in California, USA. We developed and validated generalized linear models of invasion probability to analyze the relative predictive power of 12 niche variables and a negative exponential dispersal kernel estimated by likelihood profiling. Models were developed incrementally each year (2003, 2003-2004, 2003-2005) to examine annual variability in model parameters and to create realistic scenarios for using models to predict future infections and to guide early-detection sampling. Overall, 78 new infections were observed up to 33.5 km from the nearest known site of infection, with slightly increasing rates of prevalence across time windows (2003, 6.5%; 2003-2004, 7.1%; 2003-2005, 9.6%). The pathogen was not detected in many field plots that contained susceptible host vegetation. The generalized linear modeling indicated that the probability of invasion is limited by both dispersal and niche constraints. Probability of invasion was positively related to precipitation and temperature in the wet season and the presence of the inoculum-producing foliar host Umbellularia californica and decreased exponentially with distance to inoculum sources. Models that incorporated niche and dispersal parameters best predicted the locations of new infections, with accuracies ranging from 0.86 to 0.90, suggesting that the modeling approach can be used to forecast locations of disease spread. Application of the combined niche plus dispersal models in a geographic information system predicted the presence of P. ramorum across approximately 8228 km2 of California's 84785 km2 (9.7%) of land area with susceptible host species. This research illustrates how probabilistic modeling can be used to analyze the relative roles of niche and dispersal limitation in controlling the distribution of invasive pathogens.

Human-caused changes in land use and land cover have dramatically altered ecosystems worldwide and may facilitate the spread of infectious diseases. To address this issue, we examined the influence of land-cover changes between 1942 and 2000 on the establishment of an invasive pathogen, Phytophthora ramorum, which causes the forest disease known as Sudden Oak Death. We assessed effects of land-cover change, forest structure, and understory microclimate on measures of inoculum load and disease prevalence in 102 15 x 15 m plots within a 275-km2 region in northern California. Within a 150 m radius area around each plot, we mapped types of land cover (oak woodland, chaparral, grassland, vineyard, and development) in 1942 and 2000 using detailed aerial photos. During this 58-year period, oak woodlands significantly increased in area by 25%, while grassland and chaparral decreased by 34% and 51%, respectively. Analysis of covariance revealed that vegetation type in 1942 and woodland expansion were significant predictors of pathogen inoculum load in bay laurel (Umbellularia californica), the primary inoculum-producing host for P. ramorum in mixed evergreen forests. Path analysis showed that woodland expansion resulted in larger forests with higher densities of the primary host trees (U. californica, Quercus agrifolia, Q. kelloggii) and cooler understory temperatures. Together, the positive effects of woodland size and negative effects of understory temperature explained significant variation in inoculum load and disease prevalence in bay laurel; host stem density had additional positive effects on inoculum load. We conclude that enlargement of woodlands and closure of canopy gaps, likely due largely to years of fire suppression, facilitated establishment of P. ramorum by increasing the area occupied by inoculum-production foliar hosts and enhancing forest microclimate conditions. Epidemiological studies that incorporate land-use change are rare but may increase understanding of disease dynamics and improve our ability to manage invasive forest pathogens.

Phytophthora ramorum, causal agent of sudden oak death, is an emerging plant pathogen first observed in North America associated with mortality of tanoak (Lithocarpus densiflorus) and coast live oak (Quercus agrifolia) in coastal forests of California during the mid-1990s. The pathogen is now known to occur in North America and Europe and have a host range of over 40 plant genera. Sudden oak death has become an example of unintended linkages between the horticultural industry and potential impacts on forest ecosystems. This paper examines the biology and ecology of P. ramorum in California and Oregon forests as well discussing research on the pathogen in a broader management context.

Few studies have quantified pathogen impacts to ecosystem processes, despite the fact that pathogens cause or contribute to regional-scale tree mortality. We measured litterfall mass, litterfall chemistry, and soil nitrogen (N) cycling associated with multiple hosts along a gradient of mortality caused by Phytophthora ramorum, the cause of sudden oak death. In redwood forests, the epidemiological and ecological characteristics of the major overstory species determine disease patterns and the magnitude and nature of ecosystem change. Bay laurel (Umbellularia californica) has high litterfall N (0.992%), greater soil extractable NO3 -N, and transmits infection without suffering mortality. Tanoak (Notholithocarpus densiflorus) has moderate litterfall N (0.723%) and transmits infection while suffering extensive mortality that leads to higher extractable soil NO3 -N. Redwood (Sequoia sempervirens) has relatively low litterfall N (0.519%), does not suffer mortality or transmit the pathogen, but dominates forest biomass. The strongest impact of pathogen-caused mortality was the potential shift in species composition, which will alter litterfall chemistry, patterns and dynamics of litterfall mass, and increase soil NO3 -N availability. Patterns of P. ramorum spread and consequent mortality are closely associated with bay laurel abundances, suggesting this species will drive both disease emergence and subsequent ecosystem function.

The oomycete pathogen Phytophthora ramorum is responsible for sudden oak death (SOD) in California coastal forests. P. ramorum is a generalist pathogen with over 100 known host species. Three or four closely related genotypes of P. ramorum (from a single lineage) were originally introduced in California forests and the pathogen reproduces clonally. Because of this the genetic diversity of P. ramorum is extremely low in Californian forests. However, P. ramorum shows diverse phenotypic variation in colony morphology, colony senescence, and virulence. In this study, we show that phenotypic variation among isolates is associated with the host species from which the microbe was originally cultured. Microarray global mRNA profiling detected derepression of transposable elements (TEs) and down-regulation of crinkler effector homologs (CRNs) in the majority of isolates originating from coast live oak (Quercus agrifolia), but this expression pattern was not observed in isolates from California bay laurel (Umbellularia californica). In some instances, oak and bay laurel isolates originating from the same geographic location had identical genotypes based on multilocus simples sequence repeat (SSR) marker analysis but had different phenotypes. Expression levels of the two marker genes analyzed by quantitative reverse transcription PCR were correlated with originating host species, but not with multilocus genotypes. Because oak is a nontransmissive dead-end host for P. ramorum, our observations are congruent with an epi-transposon hypothesis; that is, physiological stress is triggered on P. ramorum while colonizing oak stems and disrupts epigenetic silencing of TEs. This then results in TE reactivation and possibly genome diversification without significant epidemiological consequences. We propose the P. ramorum-oak host system in California forests as an ad hoc model for epi-transposon mediated diversification.

Phylogenetic relationships between thirteen species of downy mildew and 103 species of Phytophthora (plant-pathogenic oomycetes) were investigated with two nuclear and four mitochondrial loci, using several likelihood-based approaches. Three Phytophthora taxa and all downy mildew taxa were excluded from the previously recognized subgeneric clades of Phytophthora, though all were strongly supported within the paraphyletic genus. Downy mildews appear to be polyphyletic, with graminicolous downy mildews (GDM), brassicolous downy mildews (BDM) and downy mildews with colored conidia (DMCC) forming a clade with the previously unplaced Phytophthora taxon totara; downy mildews with pyriform haustoria (DMPH) were placed in their own clade with affinities to the obligate biotrophic P. cyperi. Results suggest the recognition of four additional clades within Phytophthora, but few relationships between clades could be resolved. Trees containing all twenty extant downy mildew genera were produced by adding partial coverage of seventeen additional downy mildew taxa; these trees supported the monophyly of the BDMs, DMCCs and DMPHs but suggested that the GDMs are paraphyletic in respect to the BDMs or polyphyletic. Incongruence between nuclear-only and mitochondrial-only trees suggests introgression may have occurred between several clades, particularly those containing biotrophs, questioning whether obligate biotrophic parasitism and other traits with polyphyletic distributions arose independently or were horizontally transferred. Phylogenetic approaches may be limited in their ability to resolve some of the complex relationships between the “subgeneric” clades of Phytophthora, which include twenty downy mildew genera and hundreds of species. [ABSTRACT FROM AUTHOR]

Phytophthora ramorum, an invasive pathogen and the causal agent of Sudden Oak Death, has become established in mixed-evergreen and redwood forests in coastal northern California. While oak and tanoak mortality is the most visible indication of P. ramorum’s presence, epidemics are largely driven by the presence of bay laurel (Umbellularia californica), a reservoir host that supports both prolific sporulation in the winter wet season and survival during the summer dry season. In order to better understand how over-summer survival of the pathogen contributes to variability in the severity of annual epidemics, we monitored the viability of P. ramorum leaf infections over three years along with coincident microclimate. The proportion of symptomatic bay laurel leaves that contained viable infections decreased during the first summer dry season and remained low for the following two years, likely due to the absence of conducive wet season weather during the study period. Over-summer survival of P. ramorum was positively correlated with high percent canopy cover, less negative bay leaf water potential and few days exceeding 30°C but was not significantly different between mixed-evergreen and redwood forest ecosystems. Decreased summer survival of P. ramorum in exposed locations and during unusually hot summers likely contributes to the observed spatiotemporal heterogeneity of P. ramorum epidemics. [ABSTRACT FROM AUTHOR]

Sudden oak death, caused by the recently described pathogen Phytophthora ramorum, is an emerging forest disease that has reached epidemic levels in coastal forests of central California. We present a rule-based model of P. ramorum establishment and spread risk in California plant communities. The model, which is being used as a management tool to target threatened forests for early-detection monitoring and protection, incorporates the effects of spatial and temporal variability of multiple variables on pathogen persistence. Model predictions are based on current knowledge of host susceptibility, pathogen reproduction, and pathogen transmission with particular regard to host species distribution and climate suitability. Maps of host species distributions and monthly weather conditions were spatially analyzed in a GIS and parameterized to encode the magnitude and direction of each variable''s effect on disease establishment and spread. Spread risk predictions were computed for each month of the pathogen''s general reproductive season and averaged to generate a cumulative risk map (Fig. 6a and b). The model identifies an alarming number of uninfected forest ecosystems in California at considerable risk of infection by Phytophthora ramorum. This includes, in particular, a broad band of high risk north of Sonoma County to the Oregon border, a narrow band of high risk south of central Monterey County south to central San Luis Obispo County, and scattered areas of moderate and high risk in the Sierra Nevada foothills in Butte and Yuba counties. Model performance was evaluated by comparing spread risk predictions to field observations of disease presence and absence. Model predictions of spread risk were consistent with disease severity observed in the field, with modeled risk significantly higher at currently infested locations than at uninfested locations (P < 0.01, n = 323). Based on what is known about the ecology and epidemiology of sudden oak death, this model provides a simple and effective management tool for identifying emergent infections before they become established. [Copyright &y& Elsevier]