Richard C. Cobb

Apparent competition in canopy trees determined by pathogen transmission rather than susceptibility

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.

Landscape epidemiology and control of pathogens with cryptic and long-distance dispersal: Sudden oak death in northern Californian forests

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 pathogens 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 pathogens 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.

A multi-species synthesis of physiological mechanisms in drought-induced tree mortality

Widespread tree mortality associated with drought has been observed on all forested continents and global change is expected to exacerbate vegetation vulnerability. Forest mortality has implications for future biosphere–atmosphere interactions of carbon, water and energy balance, and is poorly represented in dynamic vegetation models. Reducing uncertainty requires improved mortality projections founded on robust physiological processes. However, the proposed mechanisms of drought-induced mortality, including hydraulic failure and carbon starvation, are unresolved. A growing number of empirical studies have investigated these mechanisms, but data have not been consistently analysed across species and biomes using a standardized physiological framework. Here, we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought-induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves at mortality, indicating that evidence supporting carbon starvation was not universal. Reduced non-structural carbohydrates were more common for gymnosperms than angiosperms, associated with xylem hydraulic vulnerability, and may have a role in reducing hydraulic function. Our finding that hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling can be achieved using thresholds in hydraulic function.The mechanisms underlying drought-induced tree mortality are not fully resolved. Here, the authors show that, across multiple tree species, loss of xylem conductivity above 60% is associated with mortality, while carbon starvation is not universal.

Modeling when, where, and how to manage a forest epidemic, motivated by sudden oak death in California.

Significance We use sudden oak death in California to illustrate how mathematical modeling can be used to optimize control of established epidemics of invading pathogens in complex heterogeneous landscapes. We use our statewide model—which has been parameterized to pathogen spread data—to address a number of broadly applicable questions. How quickly must management start? When is an epidemic too large to prevent further spread effectively? How should local treatment be deployed? How does this depend on the budget and level of risk aversion? Where should treatment be targeted? How should expenditure be balanced on detection and treatment? What if the budget changes over time? The underlying principles are important for management of all plant disease epidemics in natural ecosystems. Sudden oak death, caused by Phytophthora ramorum, has killed millions of oak and tanoak in California since its first detection in 1995. Despite some localized small-scale management, there has been no large-scale attempt to slow the spread of the pathogen in California. Here we use a stochastic spatially explicit model parameterized using data on the spread of P. ramorum to investigate whether and how the epidemic can be controlled. We find that slowing the spread of P. ramorum is now not possible, and has been impossible for a number of years. However, despite extensive cryptic (i.e., presymptomatic) infection and frequent long-range transmission, effective exclusion of the pathogen from large parts of the state could, in principle, have been possible were it to have been started by 2002. This is the approximate date by which sufficient knowledge of P. ramorum epidemiology had accumulated for large-scale management to be realistic. The necessary expenditure would have been very large, but could have been greatly reduced by optimizing the radius within which infected sites are treated and careful selection of sites to treat. In particular, we find that a dynamic strategy treating sites on the epidemic wave front leads to optimal performance. We also find that “front loading” the budget, that is, treating very heavily at the start of the management program, would greatly improve control. Our work introduces a framework for quantifying the likelihood of success and risks of failure of management that can be applied to invading pests and pathogens threatening forests worldwide.

The phenology–substrate‐match hypothesis explains decomposition rates of evergreen and deciduous oak leaves

Summary There is substantial evidence that the rate of litter decomposition is affected by the match between the litter substrate and the soil matrix (decomposer community). We introduce and test the phenology–substrate-match hypothesis, which predicts that both litter composition and soil matrix will change over the course of the year and that a lagged match between litter type and soil matrix will result in an optimal decomposition environment. We conducted a decomposition experiment in a Mediterranean mixed deciduous–evergreen oak savanna in California. We initiated litter decomposition of both a deciduous oak (whose leaves fall in autumn) and an evergreen oak (whose leaves fall in spring) in both autumn and spring. Consistent with the phenology–substrate-match hypothesis, we found that decomposition of deciduous oak litter was accelerated compared to evergreen oak litter when decomposition was initiated in spring, while evergreen litter was accelerated compared to deciduous litter when decomposition was initiated in autumn. We also found a small effect of microsite on leaf decomposition, where both evergreen and deciduous oak leaves decomposed faster under the canopy of a conspecific. Synthesis. Our study extends theory of litter quality and the decomposer community into a temporal context, which may be an important source of variation in decomposition rates when species with different litterfall phenologies co-occur.

Research frontiers for improving our understanding of drought-induced tree and forest mortality

Accumulating evidence highlights increased mortality risks for trees during severe drought, particularly under warmer temperatures and increasing vapour pressure deficit (VPD). Resulting forest die-off events have severe consequences for ecosystem services, biophysical and biogeochemical land-atmosphere processes. Despite advances in monitoring, modelling and experimental studies of the causes and consequences of tree death from individual tree to ecosystem and global scale, a general mechanistic understanding and realistic predictions of drought mortality under future climate conditions are still lacking. We update a global tree mortality map and present a roadmap to a more holistic understanding of forest mortality across scales. We highlight priority research frontiers that promote: (1) new avenues for research on key tree ecophysiological responses to drought; (2) scaling from the tree/plot level to the ecosystem and region; (3) improvements of mortality risk predictions based on both empirical and mechanistic insights; and (4) a global monitoring network of forest mortality. In light of recent and anticipated large forest die-off events such a research agenda is timely and needed to achieve scientific understanding for realistic predictions of drought-induced tree mortality. The implementation of a sustainable network will require support by stakeholders and political authorities at the international level.

Biodiversity Conservation in the Face of Dramatic Forest Disease: An Integrated Conservation Strategy for Tanoak (Notholithocarpus densiflorus) Threatened by Sudden Oak Death

Abstract Non-native diseases of dominant tree species have diminished North American forest biodiversity, structure, and ecosystem function over the last 150 years. Since the mid-1990s, coastal California forests have suffered extensive decline of the endemic overstory tree tanoak, Notholithocarpus densiflorus (Hook. & Arn.) Manos, Cannon & S. H. Oh (Fagaceae), following the emergence of the exotic pathogen Phythophthora ramorum and the resulting disease sudden oak death. There are two central challenges to protecting tanoak: 1) the pathogen P. ramorum has multiple pathways of spread and is thus very difficult to eradicate, and 2) the low economic valuation of tanoak obscures the cultural and ecological importance of this species. However, both modeling and field studies have shown that pathogen-centric management and host-centric preventative treatments are effective methods to reduce rates of spread, local pathogen prevalence, and to increase protection of individual trees. These management strategies are not mutually exclusive, but we lack precise understanding of the timing and extent to apply each strategy in order to minimize disease and the subsequent accumulation of fuels, loss of obligate flora and fauna, or destruction of culturally important stands. Recent work identifying heritable disease resistance traits, ameliorative treatments that reduce pathogen populations, and silvicultural treatments that shift stand composition hold promise for increasing the resiliency of tanoak populations. We suggest distinct strategies for pathogen invaded and uninvaded areas, place these in the context of local management goals, and suggest a management strategy and associated research priorities to retain the biodiversity and cultural values associated with tanoak.

Litter Chemistry, Community Shift, and Non-additive Effects Drive Litter Decomposition Changes Following Invasion by a Generalist Pathogen

Forest pathogens have strong potential to shape ecosystem function by altering litterfall, microclimate, and changing community structure. We quantified changes in litter decomposition from a set of distinct diseases caused by Phytophthora ramorum, an exotic generalist pathogen. Phytophthora ramorum causes leaf blight and increased litterfall %N, but no mortality on California bay laurel (Umbellularia californica), a common overstory tree that accumulates high levels of infection. Lethal twig and bole cankers on tanoak (Notholithocarpus densiflorus) lead to the disease sudden oak death which creates canopy openings and alters litterfall in mixed-species forests dominated by redwood (Sequoia sempervirens) which is minimally susceptible. Species identity had the greatest effect on mass loss and N dynamics with the most rapid rates in bay laurel, slowest in redwood, and intermediate in tanoak. Decomposing litter from infected sources had increased N accumulation, and although these changes were of lower magnitude relative to species identity, the region-scale invasion of P. ramorum suggests that this effect could occur over an extensive area. Canopy mortality was a significant and slowing influence on litter N dynamics in all species and also dampened non-additive effects within mixed litter bags. Redwood—the lowest quality litter—demonstrated non-additive interactions with consistently lower C:N when decomposed in mixed litter bags, but this effect did not alter the entire mixture. Mortality and subsequent changes in community composition have the greatest magnitude effects on litter decomposition for sudden oak death, but our study implies that different and sometimes cryptic mechanisms will drive decomposition changes for other forest diseases.

Range-Wide Threats to a Foundation Tree Species from Disturbance Interactions

Abstract The geographic range of tanoak, Notholithocarpus densiflorus (Hook. & Arn.) Manos, Cannon & S. H. Oh (Fagaceae), encompasses tremendous physiographic variability, diverse plant communities, and complex disturbance regimes (e.g., development, timber harvest, and wildfire) that now also include serious threats posed by the invasive forest pathogen Phytophthora ramorum S. Werres, A.W.A.M. de Cock. Knowing where these disturbance factors interact is critical for developing comprehensive strategies for conserving the abundance, structure, and function of at-risk tanoak communities. In this study, we present a rule-based spatial model of the range-wide threat to tanoak populations from four disturbance factors that were parameterized to encode their additive effects and two-way interactions. Within a GIS, we mapped threats posed by silvicultural activities; disease caused by P. ramorum; human development; and altered fire regimes across the geographic range of tanoak, and we integrated spatially coinciding disturbances to quantify and map the additive and interacting threats to tanoak. We classified the majority of tanoaks range at low risk (3.7 million ha) from disturbance interactions, with smaller areas at intermediate (222,795 ha), and high (10,905 ha) risk. Elevated risk levels resulted from the interaction of disease and silviculture factors over small extents in northern California and southwest Oregon that included parts of Hoopa and Yurok tribal lands. Our results illustrate tanoak populations at risk from these interacting disturbances based on one set of hypothesized relationships. The model can be extended to other species affected by these factors, used as a guide for future research, and is a point of departure for developing a comprehensive understanding of threats to tanoak populations. Identifying the geographic location of disturbance interactions and risks to foundation species such as tanoak is critical for prioritizing and targeting conservation treatments with limited resources.