California’s Giant Coastal Forests Face a Formidable Foe

By Dane Elmquist

Figure 1. Big Sur, on the Mid-California Coastline

The drive down U.S. Highway 1 on the coast of California is one of the most paramount routes to travel in the United States. The northern half of the highway exposes motorists to beautiful landscape, with Big Sur and the California coast to the west, and diverse coastal forests to the east (Figure 1). However, expanding north from mid-California, integral parts of these giant forests are under attack by a microscopic organism that causes Sudden Oak Death (SOD), a debilitating condition that leads to mortality. The majority of oak and tanoak species affected by SOD constitutes the base structure of California’s coastal forests and are the prime targets of the agent responsible for SOD, the microbe Phytophthora ramorum. This invasive species has a wide range of hosts, but thrives in the particularly susceptible tanoaks and coast live oak ^[1]. P. ramorum has the capacity to infect 45 native California trees and foliage and has killed over 3 million oaks ^[7]. Susceptibility to infection varies in hosts, and this is an important factor for transmission and spread of SOD ^{[2] [3]}. SOD has tremendous ecological impacts in California’s coastal forests that alter forest cycles and cause loss of animal and plant diversity ^{[1] [4]}. Control measures regarding compost disposal and import of nursery plants have been created and are strictly enforced in epidemic areas. P. ramorum is responsible for recent outbreaks of SOD that have significantly impacted the west coast by causing rapid environmental changes. The microbe’s invasive nature and unknown origin continue to make it a formidable ecological threat.

Figure 2. Cankers on
infected tanoak

P. ramorum first made itself known in the mid 1990’s in Marin County, California, when alarm rose due to a large amounts of tanoaks being infected with SOD. The lack of accurate tests for detection allowed this deceptive microbe to keep its identity hidden until SOD was linked to P. ramorum in 2001 ^{[1] [3]}. Since the mid 1990’s, P. ramorum has quickly spread to 14 counties in California and one in Oregon. The evidence of P. ramorum’s presence is stark in oak trees, like coast live oak and tanoak ^[3]. These species of oak exhibit a strong reaction to P. ramorum infection results in cankers and lesions that form on the trunks that bleed a dark sap. The term “sudden oak death” comes from the speed at which the tree decays once cankers manifest. However, the cunning P. ramourm can lay dormant in a tree for years prior to developing lesions leading to a swift death ^{[5] [6]}. These cankers are often hidden beneath the bark of infected oaks because this is where P. ramorum can effectively kill the inner bark of the tree causing rapid wilting and death (Figure 2). In non-oak hosts, symptoms caused by P. ramorum include leaf spots and dieback of leaf shoots, resulting in a wilted appearance referred to as Ramorum blight ^{[3] [5]}.

Ramorum blight is critical in the transmission of SOD. The varying levels of susceptibility between host species allow P. ramorum to develop in many non-oak hosts without killing them. These plants become the perfect harbor for the dispersion of P. ramorum spores. The Bay Laurel is an especially adept transmitter for P. ramorum, with levels of infection 20 percent higher than other species in the area, but little negative effect on the Bay Laurel’s health ^{[5] [1] [8]}. The Bay Laurel’s non-lethal response to P. ramorum infection is vital for spore formation and Bay Laurel infection often precedes oak and tanoak infection. The mere presence of Bay Laurels is associated with higher levels of SOD.

P. ramorum is a fungal-like pathogen, known as a water-mold, that uses asexual reproduction to produce infectious spores; as many as 17,000 spores per lesion ^[8]. P. ramorum spores are mostly aerially dispersed making it unique in that it is the first Phytopathora to have ever been revealed with this mode of transmission. However, in heavily wooded areas this shrewd pathogen also exploits their plant victim’s life-blood—water—in order to transmit its spores. Lesions on the foliage of less susceptible hosts form at leaf tips where spores reside and propagate. As water crashes onto the forest’s leaves, P. ramorum spores are splashed off the infected leaves and diffused into the water droplets where they continue to spread ^{[9] [8] [1]}. Spores will infect a plant quicker in the presence of water and the majority of SOD infections occur during periods of heavy rainfall. High P. ramorum concentrations have been documented in streams and rainwater recently, showing that water based transmission is common ^[8]. Temperature and humidity levels are critical as well. The varying susceptibility of hosts and the increasing amount of species that act as spore reservoirs make it difficult to diagnose how P. ramorum is consistently spread. 

Figure 3. Sudden Oak Death in California coastal forests

The profound impact SOD has on the ecosystem of the coastal California forests (Figure 3) is the result of the invasive nature and ambiguous origin of the SOD architect, P. ramorum. Its identification in 2001 has spawned a dramatic increase in research on the microbe to tease out its evolutionary history and pathogenic factors. Identification of P. ramorum in European nurseries led to the belief that P. ramorum was introduced to the U.S. from imported plants. However, genetic analyses determined that each population was clonal with three genetically distinct lineages ^[13]. The three lineages were named with respect to their location of discovery in Europe or North America (EU1, NA1, and NA2). NA1 is the main lineage that causes SOD in coastal forests, but EU1 and NA2 are considerable pathogenic lineages in nurseries ^[5]. Knowledge of the different P. ramorum lineages has led to questions regarding variation in the genome and proliferation of disease.

P. ramorum’s genome sequence (NA1) was published in 2006 allowing in depth genomic evaluation. Isolates from California and Oregon were determined to be phenotypically different and displayed varying levels of pathogenicity ^[14]. The phenotypic differences between strains are caused by transposable elements, DNA sequences that can alter their position in the genome, permitting novel mutations that affect phenotypic traits like infection ability ^[15]. Transposable elements are linked with the evolution of specific lineages, like EU1, NA1, NA2, typified by changes in hosts and environmental interactions. Phenotypic differences among isolates were determined to be the result of the host species they propagated on ^[15]. These transposable elements are shut off in the genome until pathogenic stress in the host activates the transposable elements in P. ramorum’s genome. This results in the diversification of pathogenicity seen in P. ramorum. 

The recent discovery of the P. ramorum pathogen and SOD means that the long-term ecological impacts on the region have yet to be realized. However, the northern California ecosystem has already been affected by SOD. Aside from massive dieback of oak and tanoak populations, common geochemical cycles are also being effected by SOD. Fire has a historic role in forest ecosystems and the new invasive P. ramorum copes with this dominant ecological process. Studies reveal that oaks recently infected with SOD burned more intensely than oaks infected for a longer time ^[10]. The rapid accumulation of dead foliage in response to P. ramorum infection is the reason for differences in fire intensity. Despite the tremendous power of fire, the majority of the ecological impact caused by P. ramorum in forests comes in the wake of the flames. SOD infected oaks play host to a variety of beetles that occupy and drastically reduce the survival time of infected trees. Wildfires in forest regions infected with SOD were linked to a higher density of these oak bark beetles ^[11]. 

SOD also decreases biodiversity in affected areas. Tanoaks and other oak species play the primary structural role in California’s coastal forests and their decline affects many organisms that depend on the trees for food, habitat, and completion of biological processes. Squirrels and birds dependent on acorns produced by tanoaks are experiencing reduced food sources. Insects common to the forests are disappearing due to habitat loss and consequently native insectivorous birds are experiencing food source reduction. Unique fungi that depend on the oaks to complete vital decomposition and nutrient cycling in the forest will be wiped out ^[6]. Changes in soil dynamics and composition due to increased nitrogen levels are also contributed to P. ramorum and SOD ^[12]. The highly susceptible tanoak, which many vertebrates depend on for food, does not regenerate proficiently in SOD epidemic areas. This causes an ecosystem-wide shift, allowing the propagation invasive species and Bay Laurels that were otherwise outcompeted. As mentioned before, high tanoak mortality rates also increase the dead foliage used as fuel for wildfires. Non-tanoak hardwood species are able to regenerate, but species like the redwood do not supply an abundant food source and are still unable to fully occupy the gaps left by tanoak mortality due to SOD ^[4].

The uncertain evolutionary history and complex genetics of P. ramorum make this newly identified plant pathogen intriguing to researchers, naturalists, and governments. Since 2000, millions of dollars have been invested in research and control of SOD ^[3]. Discovery of all three lineages in California nurseries reinforces the fact that control of commercial plant trade is vital to pathogen quarantine efforts ^[5]. Regulations in 14 California counties have been enacted to stop the spread of SOD. Citizen science efforts are being employed to track the infection. Coupled with scientific efforts to identify the origin and varying phenotypic qualities of P. ramorum, control of this eukaryotic pathogen is coming to fruition in California and the US. Understanding the P. ramorum and host ecology of the forest is critical to controlling SOD. Interactions between fire and other biotic factors in forest growth, spread of P. ramorum through multiple hosts with varying susceptibility, and genetic clues about pathogenic variation in P. ramorum will be the key in Sudden Oak Death control and search for a solution.

References

[1] Rizzo, D., Garbelotto, M., and Hansen, E. 2005. Phytophthora ramorum: Integrative Research and Management of an Emerging Pathogen in California and Oregon Forests. Annual Review of Phytopathology. 49. p. 309-335.

[2] Davidson, J. M., Patterson, H. A., Wickland, A. C., Fichtner, E. J., and Rizzo, D. M. 2011. Forest type influences transmission of Phytophthora ramorum in California oak woodlands. Phytopathology 101. p. 492-501.

[3] Matt, Daughtery, and Hung Kim. "Sudden Oak Death." Center for Invasive Species Research. University of California Riverside, 16 May 2013. Web. 20 Nov 2013. <http://cisr.ucr.edu/sudden_oak_death.html>

[4] Ramage, B.S.; O’Hara, K.L; and Forrestel, A.B. 2011. Forest transformation resulting from an exotic pathogen: regeneration and tanoak mortality in coast redwood stands affected by sudden oak death. Canadian Journal of Forest Research. 41.p.763-772.

[5] GRÜNWALD, N. J., GOSS, E. M. and PRESS, C. M. 2008. Phytophthora ramorum: a pathogen with a remarkably wide host range causing sudden oak death on oaks and ramorum blight on woody ornamentals. Molecular Plant Pathology. 9. p. 729–740. doi: 10.1111/j.1364-3703.2008.00500.x

[6] Rizzo, D., Garbelotta, M. 2003. Sudden Oak Death: Endangering California and Oregon Forest Ecosystems. Frontiers in Ecology and the Environment Vol. 1, No. 4 pp. 197-204

[7] Kuljian, H., Morgan Varner, J. 2010The effects of sudden oak death on foliar moisture content and crown fire potential in tanoak. Forest Ecology and Management. Volume 259, Issue 10, 30. p. 2103-2110, ISSN 0378-1127.http://dx.doi.org/10.1016/j.foreco.2010.02.022.

[8] Davidson, J. M., Patterson, H. A., Wickland, A. C., Fichtner, E. J., and Rizzo, D. M. 2011. Forest type influences transmission of Phytophthora ramorum in California oak woodlands. Phytopathology.101. p. 492-501.

[9] Davidson, J. M., Patterson, H. A., and Rizzo, D. M. 2008. Sources of inoculum for Phytophthora ramorum in a redwood forest. Phytopathology. 98. p. 860-866.

[10] Metz, M., Frangioso, K., Meentemeyer, R., Rizzo, D. 2011. Interacting disturbances: wildfire severity affected by stage of forest disease invasion. Ecological Applications. 21. p. 313–320. http://dx.doi.org/10.1890/10-0419.1

[11] Beh, Maia M.; Metz, Margaret; Seybold, Steven J.; Rizzo, David. 2013. The novel interaction between Phytophthora ramorum and wildfire elicits elevated ambrosia beetle landing rates on tanoak. In: Frankel, S.J.; Kliejunas, J.T.; Palmieri, K.M.; Alexander, J.M. tech. coords. Proceedings of the sudden oak death fifth science symposium. Gen. Tech. Rep. PSW-GTR-243. Albany, CA: U.S. Department of Agriculture, Forest Service, Pacific Southwest Research Station: p. 123.

[12] Cobb, R. C., Eviner, V. T. and Rizzo, D. M. 2013. Mortality and community changes drive sudden oak death impacts on litterfall and soil nitrogen cycling. New Phytologist, 200. p. 422–431. doi: 10.1111/nph.12370

[13] Ivors K, Garbelotto M, Vries ID, Ruyter-Spira C, Te Hekkert B, Rosenzweig N , Bonants P 2006. Microsatellite markers identify three lineages of Phytophthora ramorum in US nurseries, yet single lineages in US forest and European nursery populations. Molecular Ecology. 15(6). p.1493-505

[14] Huberil, D. Harnik, T.Y., Meshriy, M., Miles, L. and Garbelotto, M. 2006. Phenotypic variation among Phytophthora ramorum isolates from California and Oregon. Sudden oak death second science symposium: the state of our knowledge, Pacific Southwest Research Station. Source:OAI.

Figure Sources

Figure 1. Buyers Brokerage Real Estate. <http://www.thebuyersbrokerage.com/big-sur-real-estate>

Figure 2. Matt, Daughtery, and Hung Kim. "Sudden Oak Death." Center for Invasive Species Research. University of California Riverside, 16 May 2013. Web. 20 Nov 2013. <http://cisr.ucr.edu/sudden_oak_death.html>

Figure 3. U.S. Forest Service. Sudden Oak Death Research - Phytophthora ramorum. 2011. http://www.fs.fed.us/psw/partnerships/sod/