Whitebark pine is a keystone species in high-elevation areas of western North America due to its influence on biodiversity, ecosystem structure, and hydrologic cycles [1
]. The species’ survival is threatened by an introduced pathogen (Cronartium ribicola
J. C. Fisch) that was first documented in western North America in 1910 [3
]. C. ribicola
is a fungus that can infect all five-needled pines, causing the white pine blister rust disease (WPBR). The fungus requires an alternate host to complete its life cycle including several species of Ribes
, and Pedicularis
, which are all widely distributed in the subalpine ecosystems [5
]. Over the last 100 years, precipitous declines and widespread mortality have been documented in whitebark pine across the western United States and western Canada. In addition to WPBR, other factors implicated in the species’ decline include changing fire regimes, mountain pine beetle (Dendroctonus ponderosae
Hopkins), and warming climates [6
]. Currently, whitebark pine is listed as a candidate for protection under the U.S. Federal Endangered Species Act and as endangered under the Species at Risk Act (SARA) in Canada [11
Historical accounts of the spread of WPBR from areas near North Cascades National Park Service Complex are limited to one 1913 report of a potential pine infection near Newhalem, Washington on the west edge of the park [4
]. In contrast, Mount Rainier National Park was a center of activity from the late 1920s through the 1960s. Despite widespread Ribes
eradication programs, 52–55% of whitebark pines in the Sunrise area (Figure 1
) were recorded as infected in 1952. In the late 1950s and 1960s, work in Mount Rainier National Park turned to treatment with fungicides and surveys for western white pine that appeared to have genetic resistant to WPBR. Although the scenic value of whitebark pine was repeatedly mentioned in park memos, efforts to control WPBR through fungicides and Ribes
removal were terminated around 1964 when it was determined neither tactic was effective in reducing the spread of WPBR [13
Between 1994 and 1999, national park staff conducted inventories in both parks to quantify the incidence of WPBR and mountain pine beetle in whitebark pine stands [15
]. Surveys revealed that about one third of all trees surveyed were dead, incidence of WPBR infection was highly variable (0–70%), and observations of mountain pine beetle were rare. Contemporaneous studies conducted in the Washington and Oregon Cascades documented similar patterns: high variability among sites, limited mountain pine beetle activity, WPBR infection of live trees ranging from 4.7–73%, and mortality ranging from 10–23% [8
]. All studies noted difficulty in attributing the cause of mortality since many trees had been dead for many years.
Following initial inventories, we realized that long-term monitoring plots with marked trees were needed to attribute the cause of mortality and to track long-term trends in population health [6
]. In 2004, we established permanent plots in each park to document status and trends in whitebark pine population health and to provide a foundation of scientific data to inform national park conservation strategies and management tactics. Specifically, our objectives were: (1) describe the current composition and structure of whitebark pine stands; (2) quantify status and trends in incidence of WPBR infection and mortality in trees and saplings; (3) quantify the incidence of mountain pine beetle; (4) describe status and trends in seedling density; and (5) evaluate landscape patterns of WPBR infection and whitebark pine mortality.
4. Discussion and Conclusions
The results of our study increase the spatial and temporal resolution of knowledge on the status and trends in whitebark pine population health in the Cascade Mountains. The incidence of infection (18–32%) and mortality (7–38%) that we documented in 2004 were similar in range to those recorded on adjacent forest lands by Shoal and Aubry in 2004–2005 (infection 5–73% and mortality 1–61%) [17
] and British Columbia by Campbell and Antos in 1994–1995 (blister rust incidence 27–44% and mortality about 21%) [26
]. In all three studies, mountain pine beetle presence was rare and WPBR was thought to be the primary cause of mortality. Over the course of our study, we had increasing confidence in WPBR as the primary cause of mortality because: (1) it was the primary agent of damage to whitebark pine, (2) evidence of mountain pine beetle was observed in few trees, (3) we saw no evidence of stand-replacing fires, and (4) trees that died after they were tagged in 2004 had bole or stem cankers present in previous surveys.
Although Shoal and Aubry reported north-south and west–east trends in the incidence of blister rust infection reflecting gradients in temperature and precipitation from Washington to Oregon [17
], these trends were not apparent in our study. Our study was conducted across a smaller geographic scale and may indicate that environmental conditions are generally favorable for WPBR spread throughout our parks [26
]. We found incidence of infection and mortality were higher on south and east aspects and mortality decreased with elevation. Decreasing mortality with elevation could reflect fewer frost free days, hence a shorter growing season for whitebark pine producing a lag between infection and mortality with slower disease progression from needle to tree bole [10
]. Or, the decrease in frost free days could limit spore production and spread from alternate hosts to whitebark pine [26
Over the 12 years since we initiated our study, the percent of whitebark pine infected with WPBR and the percent of dead whitebark pine increased in all of our study sites. Although annualized mortality rates decreased between monitoring periods, the prevalence of WPBR infection and mortality increased across our park landscapes. With each survey period, the number of whitebark pine trees in our study sites decreased and natural regeneration was limited. Initially, incidence of WPBR and mortality were highest in larger diameter classes, but with each successive survey, smaller diameter trees also became infected or died. When we modeled prevalence of WPBR infected trees and dead whitebark pine trees on the landscape, we found that diameter and year were the most important variables rather than site or park, and with each survey year the prediction of prevalence increased in all diameter classes.
Our study results indicate that the primary driver of whitebark pine decline in our two parks is WPBR. Ettl and Cottone [27
] developed a spatially explicit model of whitebark pine for Mount Rainier National Park using dendrological estimates of growth and mortality and predicted that there would be fewer than 100 trees left in the park in 148 years. As we begin to develop long-term strategies for managing whitebark pine in our parks, we need to consider levels and frequency of genetic resistance to WPBR and the influence of changing climates on stand dynamics [28
]. Since WPBR was introduced over 100 years ago, some of the older surviving trees may be indicative of resistance to WPBR. We are screening progeny from cones collected in Mount Rainier and North Cascades at the USDA Forest Service Dorena Genetic Resource Center for resistance and have found moderate levels of genetic resistance in Mount Rainier National Park families and high genotypic diversity in samples from both parks [29
]. Progeny of parent trees from Mount Rainier National Park have shown among the highest levels of genetic resistance to WPBR of any geographic sources to date in seedling inoculation trials [30
]. But our cone collections have been limited in geographic scope and should be expanded to provide an accurate picture of the frequency of resistance. We also need to conduct field trials to validate the results of seedling inoculation trials to inform restoration prescriptions (Sniezko, per. comm).
In our surveys, we found that whitebark pine was a minor component of fairly diverse tree stands. With each successive survey, the number of reproductive whitebark pine trees decreased and natural regeneration was dominated by subalpine fir. Many sites in our surveys had no whitebark pine seedlings or saplings, and maximum sapling density was only 343 stems/ha. In some sites, density of subalpine fir saplings was over 6000 stems/ha and seedling densities were over 14,000 stems/ha. McCaughey et al. [31
] recommended planting hardy seedlings from potentially rust-resistant trees at a density of 479 stems/ha, based on an assumption of 50% survival. The seedling and sapling densities at our sites are not high enough to perpetuate whitebark pine even without considering competition from other species. We do not have enough detailed information from our surveys to ascertain why we have such low levels of regeneration. Visiting sites every five years has not provided enough information on cone crop size or periodicity. Several studies have reported that dispersal by Clark’s nutcrackers is a function of the cone density to attract nutcrackers and available canopy openings for seed caching [32
]. In fact, Ray et al. [37
] recently documented that abundance of Clark’s nutcrackers is strongly decreasing in Mount Rainier National Park and appears to be decreasing in North Cascades National Park Service Complex. It would be advantageous if future surveys were conducted more frequently to record cone production and include documentation of canopy openings as a means of evaluating the potential for dispersal of seeds by Clark’s nutcrackers.
As we consider management strategies to preserve whitebark pine on our landscapes, the influence of climate change adds to the complexity of our management [28
]. Warmer summers and lower snowpack will facilitate the establishment of more trees in subalpine ecosystems [38
], increasing competition in the overstory and regeneration stratum. If lodgepole or western white pine distributions expand, mountain pine beetle may become a stronger driver of whitebark pine mortality. Fire frequency, size, and severity are projected to increase with warming climates and may prepare new areas for regeneration, entirely remove stands, or in areas where fire is excluded, it may result in lower densities of whitebark pine regeneration [38
]. Warmer, drier climates could also influence patterns of mortality and infection if north aspects become more suitable for WPBR reproduction and infection of WBP [35
Patterns in prevalence, mortality, infection, and regeneration are highly variable across our park landscapes, pointing toward the need for increased monitoring, more genetic resistance screening, and development of site specific restoration plans that include active management alternatives such as planting. The National Park Service Organic Act states that the responsibility of the National Park Service (NPS) is to conserve park resources unimpaired for future generations [41
]. Loss of whitebark pine, from WPBR, threatens to change ecosystem processes and the trajectory of these ecosystems [1
]. In 2012, the National Park Service Advisory Board recommended that the National Park Service should “…steward NPS resources for continuous change that is not yet fully understood…” to protect ecological integrity while relying on the best available sound science [42
Whitebark pine was listed as a candidate species by the US Fish and Wildlife Service under the US Endangered Species Act (ESA) in 2011 and as endangered in 2012 under Canada’s Species at Risk Act [11
]. Currently, a collaborative effort to develop a Range-wide Whitebark Pine Restoration Plan is underway [43
]. Most of the whitebark pine in the US is distributed on federal lands, and many of these lands are designated Wilderness. NPS policies support science-based management and continuous change in naturally evolving levels of genetic diversity and ecosystem function. Protection of whitebark pine populations may require hands-on restoration tactics that could appear at odds with the paradigm of Wilderness management [44
]. Protected lands managers will need to re-examine how Wilderness areas are managed in light of the severity and rate at which introduced species, in combination with changing climates, are altering these landscapes.