- Top of page
- Materials and Methods
- Supporting Information
Disturbance is a key component of many forest ecosystems (Pickett & White, 1985). However, in addition to natural disturbances (e.g. wildfire), many forests are now being transformed by accelerated climate change, biological invasions and habitat change (Turner, 2010). As these novel disturbances proliferate, more long-term effects and qualitative changes to forest ecosystems are expected (Lovett et al., 2006; Turner, 2010). Novel disturbances may interact with historically recurring disturbances in unknown ways with the potential to alter landscape structure and function (Buma & Wessman, 2011). In spite of these consequences, changing and interacting disturbance regimes have received little attention relative to other drivers of ecosystem change (Turner, 2010).
Interactions between invasive forest pests and wildfire are currently of great relevance in the USA. From 1990 to 2006, there was a nearly three-fold increase in the detection rate of established ‘high impact’ forest pathogens and insects (those species of regulatory significance or that have caused notable damage to forest trees) compared with the previous 130 yr (Aukema et al., 2010). In addition, the frequency of large wildfires in the western USA has increased significantly since the mid-1980s, together with warming temperatures and lengthened fire seasons (Westerling et al., 2006). Although there is a growing body of literature on interactions between forest insects and wildfire (e.g. McCullough et al., 1998; Parker et al., 2006; Jenkins et al., 2008), there have been few studies on the interactions between forest pathogens and fire. Those that do exist have focused primarily on native pathogens and the use of prescribed burning in managed forest systems. Examples include the burning of longleaf pine (Pinus palustris) seedlings in the southern USA to reduce brown spot needle blight (causal agent Mycosphaerella dearnessii), and the stimulation of conifer root rot infections by Rhizina undulata following fires or brush burning (Ahlgren, 1974; Hardison, 1976; Parmeter, 1977). However, research on the interactions between non-native pathogens and wildfires is extremely limited. Given that exotic pathogens have not co-evolved with their new hosts or the local disturbance regimes, these types of interactions may be some of the most unpredictable.
Coastal forests of California are part of a Mediterranean ecosystem that includes wildfire as a natural component of its disturbance regime. These forests are now coping with a new disturbance: Phytophthora ramorum, the introduced pathogen that causes sudden oak death (SOD), has killed millions of tanoaks (Notholithocarpus densiflorus) and oaks (Quercus spp.) (Rizzo et al., 2002, 2005; Meentemeyer et al., 2011). Symptoms of SOD were first noted in the San Francisco Bay area in the mid-1990s, but P. ramorum has since spread over a 700-km range from central California to southwestern Oregon (Rizzo et al., 2002, 2005). Within P. ramorum-infested areas of coastal California, the historical role of wildfire is not well characterized and appears to be highly variable across different regions and forest types (Davis & Borchert, 2006; Van de Water & Safford, 2011). In the current era of fire suppression and management, however, fire frequencies and sizes are actually increasing in some areas near the limits of P. ramorum's current range in California (Moritz & Odion, 2005; Davis & Borchert, 2006; Stuart & Stephens, 2006). As the native range of P. ramorum remains uncertain (Goss et al., 2009), it is unknown whether this pathogen may have evolved with wildfire.
Wildfire and P. ramorum may interact directly or indirectly. Wildfire could directly eliminate the pathogen from burned areas. In contrast, each disturbance may change the forest structure in ways that influence indirectly the frequency, prevalence or severity of the other disturbance. Selective host mortality by P. ramorum may affect the accumulation of woody fuels and fire severity (Metz et al., 2011; Valachovic et al., 2011), whereas differential susceptibility to fire among important host species (Fites-Kaufman et al., 2006) has feedbacks for disease prevalence.
The summer of 2008 brought the first wildfires to occur in known P. ramorum-infested forests in California, with the largest fire burning in the Big Sur region (Monterey County) (Metz et al., 2011). More than 100 000 ha were burned in Big Sur, including large portions of our long-term forest plot network established to study feedbacks between P. ramorum, its various hosts and the physical environment (Haas et al., 2011; Metz et al., 2011, 2012). Big Sur is one of the most ecologically diverse areas in California, and its forests are among the earliest infested and most impacted by SOD (Mascheretti et al., 2008; Meentemeyer et al., 2008). Tanoak mortality in some forest stands exceeds 60% and, across the Big Sur ecoregion, P. ramorum has killed hundreds of thousands of host trees (Maloney et al., 2005; Meentemeyer et al., 2008).
In this study, we capitalize on the natural experiment presented by the 2008 fires to examine the direct and indirect impacts of wildfire on the persistence of P. ramorum in Big Sur. Specifically, we address three questions: first, did the 2008 wildfires eradicate P. ramorum from areas known to have been infested before the fires? Second, if the wildfires did not eradicate the pathogen, under what conditions was P. ramorum able to persist in forest stands despite fire? And third, what are the likely reservoirs for pathogen persistence and re-invasion? We hypothesized that the detection of P. ramorum in the burned landscape would be negatively affected by high burn severities, and influenced by forest type and prevalence of host species. The results of this study provide much needed information on the poorly understood, but increasingly important, topic of interacting disturbances.
- Top of page
- Materials and Methods
- Supporting Information
The 2008 Big Sur wildfires suppressed, but did not eradicate, P. ramorum from vegetation in areas that were previously infested. We were able to recover P. ramorum 1 and 2 yr post-fire in burned plots of both forest types, and, in some cases, with no difference in frequency than in unburned plots. However, P. ramorum recovery 1 yr after the wildfires tended to take place in plots with the lowest burn severities, whereas pathogen recovery 2 yr post-fire occurred in plots with greater burn severities and was largely influenced by high levels of pre-fire disease prevalence and low levels of post-fire bay laurel mortality (Table 1, Figs 2, 3). In plots in which P. ramorum was not recovered even 2 yr post-fire, burn severities and levels of post-fire bay laurel mortality tended to be high (Table 1, Fig. 3). In summary, multiple interacting biotic and abiotic factors were responsible for the persistence of P. ramorum in previously infested burned plots. Just as the establishment, spread and survival of P. ramorum in the absence of fire is dependent on the biological and physical environment, host susceptibility and attributes of the pathogen (Rizzo et al., 2005), these same types of characteristics influenced pathogen survival and re-establishment in burned forests.
Impacts of fire on P. ramorum and its hosts
As a result of direct lethality of fire or of fire's consumption of P. ramorum's required hosts, the pathogen was detected in only one-fifth of the burned plots in the first year following wildfire. Although flame temperatures from wildfires can reach 1400°C, and temperatures in the combustion zone can reach 1000–1200°C (DeBano et al., 1998), P. ramorum is known to survive exposure to fairly high temperatures (Harnik et al., 2004; Swain et al., 2006; Tooley et al., 2008), and thus it is conceivable that the pathogen could have persisted in host tissues that survived the fires. Furthermore, host tissues probably provide a level of heat protection for P. ramorum (Harnik et al., 2004; Swain et al., 2006). Smoke produced by wildfires has also been suggested as a potential mechanism for the inhibition of fungal pathogens (Parmeter & Uhrenholdt, 1975) and P. ramorum (Moritz & Odion, 2005), but our recovery of the pathogen in heavily burned areas, which were surely exposed to large amounts of smoke, indicates that smoke probably has little residual effect on P. ramorum growth.
Fire-caused mortality of P. ramorum hosts, especially bay laurel, probably had the most significant impact on pathogen survival. In burned plots, foliage was dead and scorched, tree crowns were dead or dying as a result of cambial damage, and entire trees were consumed in the fires. It is unlikely that P. ramorum would be able to subsist in these incinerated trees, regardless of whether it survived the high temperatures of the fires. However, the pathogen was not recovered post-fire from some unburned plots that were previously known to be infested, and it was readily recovered from some plots that suffered severe fire effects. These exceptions indicate that fire, burn severity and post-fire mortality of hosts are not the only variables affecting P. ramorum survival in Big Sur.
Despite the reduced chance of recovering P. ramorum from burned plots, pathogen isolation frequency from bay laurel in unburned plots was no greater than that from burned plots in 2009, and both were lower than the detection frequencies from four California counties in 2002–2003 (42–69% per plot in pathogen-infested, unburned areas; Maloney et al., 2005). The poor P. ramorum isolation frequency from unburned plots in 2009 was possibly a result of unfavorable conditions for growth, sporulation and infection (Garbelotto et al., 2003). Rainfall levels in the central coast region were c. 50% of average over 2007–2009, and 2008 had the driest spring of the last 114 yr (California Department of Water Resources, 2010a). Increased pathogen isolation frequency and number of P. ramorum-positive plots in 2010 reflected both post-fire re-establishment of the pathogen and changing weather conditions. Water content in California's mountain snowpack was 143% of normal at the end of April 2010 (California Department of Water Resources, 2010b), signaling an end to the 3-yr drought in the region. With the onset of conditions more conducive to P. ramorum growth and the increasing quantities of host tissue available for potential infection, pathogen recovery from redwood plots increased greatly in 2010.
Pathogen persistence and re-colonization
One potential survival mechanism for P. ramorum in areas with high burn severities could be partially a function of the wildfires themselves. Patchy burn patterns that result in ‘green islands’ are typical of mixed-severity fires with variable burn intensities (Fites-Kaufman et al., 2006; Perry et al., 2011). Even one dominantly situated P. ramorum-infected sporulating host could provide sufficient inoculum to re-infest post-fire re-growth in a plot (Fig. 4). Similar scenarios involving surviving dwarf mistletoe-infected pines in burned forests have resulted in dwarf mistletoe infections in newly regenerated stands (Parmeter, 1977).
Figure 4. Photograph of a bay laurel tree in a ‘green island’ (indicated by the arrow) created by the patchy burn patterns of the 2008 wildfires in the Big Sur region. Prolific basal and epicormic sprouting can also be seen on the burned trees in this photograph.
Download figure to PowerPoint
In Big Sur, we observed that large numbers of pre-fire P. ramorum-infected bay laurel increased the likelihood of pathogen recovery post-fire, presumably because there was a greater chance that at least one of these trees would be spared the flames and serve as a refugium for the pathogen. Indeed, surveys in 2009 documented a number of surviving bay laurel ‘green islands’ in burned plots, which probably provided an important source of post-fire inoculum. Not only are attached bay laurel leaves thought to be the best niche for P. ramorum survival during adverse conditions, such as hot, dry California summers, but they also support the highest sporulation rates of forest trees in California and produce the bulk of P. ramorum inoculum in mixed-evergreen forests (Davidson et al., 2005, 2008, 2011).
By the first summer post-fire, there was already a proliferation of new vegetative growth (mainly basal sprouts) in burned plots. Young host tissues have been shown to be more susceptible than mature host tissues to P. ramorum infection (Hansen et al., 2005), yet we found relatively low P. ramorum isolation frequency from young bay laurel basal sprouts in burned plots. In contrast, the high incidence of P. ramorum-infected tanoak basal sprouts in burned plots in 2009 came as no surprise. The susceptibility of this type of host tissue to P. ramorum infection following controlled burns in Oregon was found to be so severe that the pathogen eradication protocol was amended to include the use of herbicides on tanoak sprouts following fire to help prevent the re-establishment of the pathogen in treated areas (Hansen & Sutton, 2006; Goheen et al., 2009). These findings suggest that the copious tanoak basal sprouts that arise after fire are important to the re-establishment of P. ramorum in forest types in which this host is particularly abundant, such as redwood forests of coastal California and Douglas fir–tanoak forests of southwestern Oregon. Phytophthora ramorum has also been detected in soil adjacent to stumps of previously infected trees at controlled-burn eradication sites in Oregon (Goheen et al., 2009), as have other forest Phytophthora species following prescribed fires or wildfires (see Marks et al., 1975; Hardison, 1976; Betlejewski, 2009; Meadows et al., 2011), but it is unclear whether P. ramorum soil inoculum plays an important role in the re-establishment of this predominantly aerial, splash-dispersed pathogen.
One unexpected discovery from this study was how frequently two other non-native Phytophthora species, P. pseudosyringae and P. nemorosa, were isolated from bay laurel basal sprouts in burned mixed-evergreen plots. Both species are also found throughout the range of P. ramorum and beyond, yet neither had previously been detected in any of the plots included in this study. Given that P. ramorum recovery was low from bay laurel basal sprouts in burned plots, our findings suggest that P. pseudosyringae and P. nemorosa enjoyed a competitive advantage over P. ramorum in this particular niche. The ecology of P. pseudosyringae and P. nemorosa is deserving of more attention, especially as infrequently detected invasive species can emerge as serious pathogens under varying environmental conditions (Linzer et al., 2009).
Implications for management of the pathogen
The persistence and re-establishment of P. ramorum in 2 yr following large-scale wildfires demonstrate that fire is not a panacea for the control of this forest pathogen. Just as controlled burns have been ineffective in the eradication of P. ramorum in infested forests of southwestern Oregon (Goheen et al., 2009) and California (Lee, 2009), it is unlikely that fire will serve as a natural control of P. ramorum, except over very short time frames. Factors that aid P. ramorum's persistence in burned areas are some of the same attributes that make it successful as an invasive pathogen in California's coastal forests: aerial dispersal of spores, the pathogen's ability to utilize multiple hosts in mixed-forest communities and the hosts’ propensity for vegetative sprouting following disturbance. Exotic pests and pathogens, if they manage to become established in an area, usually remain as permanent components of that ecosystem (Lovett et al., 2006), and this seems to be the case with P. ramorum in the Big Sur ecoregion.
The dynamic nature of landscapes, together with the rapid increase in biological invasions, climate shifts and human exploitation of resources, make it difficult to predict the response of an ecosystem to disturbance (Turner, 2010). In the midst of such change, the use of field-based studies is essential for a full understanding of the range of ecological impacts and feedbacks caused by disturbance. The results of this study, combined with those of Metz et al. (2011), reveal complexities of interacting biotic and abiotic disturbances in the heavily disease-impacted Big Sur landscape that a modeling study would be hard pressed to capture. Continued and ongoing surveys in Big Sur will provide additional information on P. ramorum re-establishment following fires, host mortality trends and the effects of competing Phytophthora species in the post-fire landscape.